
==== Front
Curr Res Food Sci
Curr Res Food Sci
Current Research in Food Science
2665-9271
Elsevier

S2665-9271(24)00148-5
10.1016/j.crfs.2024.100822
100822
Review Article
Sporolactobacillus—a new functional genus with potential applications
Guo Xinyu 6220112024@stu.jiangnan.edu.cn
ab
Yu Leilei ab
Xiao Meifang ab
Zang Xiaojie ab
Zhang Chengcheng ab
Narbad Arjan c
Chen Wei abd
Tian Fengwei fwtian@jiangnan.edu.cn
ab⁎
Zhai Qixiao ab
a State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi, Jiangsu, 214122, PR China
b School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, 214122, PR China
c Quadram Institute Bioscience, Norwich Research Park Colney, Norwich, Norfolk, NR4 7UA, UK
d National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, Jiangsu, 214122, PR China
⁎ Corresponding author. State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi, Jiangsu, 214122 PR China. fwtian@jiangnan.edu.cn
14 8 2024
2024
14 8 2024
9 10082214 3 2024
2 8 2024
13 8 2024
© 2024 The Authors. Published by Elsevier B.V.
2024

https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by-nc/4.0/).
Sporolactobacillus is a genus of lactic acid bacteria, which can be widely found in soil. According to NCBI, only 20 strains of the genus Sporolactobacillus have been identified through phenotypic and genotypic analysis, indicating their relatively low numbers compared to other lactic acid bacteria. Currently, there is a growing interest in isolating and studying Sporolactobacillus, particularly focusing on its physiological characteristics and conducting in vitro experiments. This paper provides a review of the sources and physiological characteristics of Sporolactobacillus, along with genotype analysis, carbohydrate metabolism traits, and potential antibacterial properties. It also delves into basic physiological characteristics, lactic acid production, and applications, offering insights for the future utilization of Sporolactobacillus and laying a foundation for exploring its potential applications.

Graphical abstract

Image 1

Highlights

• 112 CAZymes and 29 bacteriocins are found in the 20 strains of Sporolactobacillus according to the genotype analysis.

• Sporolactobacillus exhibits diverse traits including acid and bile resistance, and heat resistance.

• Sporolactobacillus has a strong ability to produce phenyllactic acid and polylactic acid.

Keywords

Sporolactobacillus
Genomic analysis
Lactic acid
Phenyllactic acid
Handling Editor: Siyun Wang
==== Body
pmc1 Introduction

Food and Agriculture Organization(FAO)/World Health Organization(WHO) defines probiotics as “live microorganisms that confer health benefits on the host when administered in an adequate amount” (Kamada et al., 2014). In recent years, the effects of probiotics on human health and disease have garnered increasing attention. However, present studies on probiotics mainly focus on traditional probiotics, such as Lactobacillus, Bifidobacterium, Streptococcus (Duc et al., 2004), and some yeasts (Islam, 2016). Studies show that traditional probiotics do not survive in harsh environments (Keller et al., 2019). The development of strains that can survive in harsh environments and exhibit required biological activity is a hot topic for research nowadays, placing spore-producing microorganisms in the spotlight, as they cannot be used as probiotics as widely as traditional probiotics, but their survival rate and stability are much higher due to the spores they produce. Therefore, the development of spore-producing bacteria with potential probiotic effects is an ideal option (Fares et al., 2015).

In 1967, Kitaharael et al. (Kitahara and Suzuki, 1963) isolated a bacterial strain from chicken feed that was bacteriophage-producing, peroxidase-negative, and capable of flagellar motility. The isolated bacterium metabolized sugars by homofermentation, producing D-lactic acid, similar to Lactobacillus; therefore, the newly isolated bacterium was assigned as a subgenus of Lactobacillus and named Sporolactobacillus. However, due to its spore-producing properties, this bacterium was later assigned to the genus Sporolactobacillus (Kitahara and Lai, 1967). In 1972, Sporolactobacillus was assigned under the family Bacillaceae (Kitahara and Toyota, 1972). Differences between Sporolactobacillus and Lactobacillus have been discovered through DNA–DNA hybridization (Dellaglio et al., 1975). In the new edition of Bergey's bacteriological identification manual, the genus Sporolactobacillus has been placed under Kingdom Bacteria, phylum Firmicytes, and family Sporolactobacillaceae, with Sporolactobacillus inulinus as an example species. The strains of Sporolactobacillus genus exhibit the capability to produce antibiotics, enzymes, and probiotics, which confers significant economic potential in the pharmaceutical, agricultural, and food industries (Alexandri et al., 2019). Furthermore, Sporolactobacillus can efficiently produce D-lactic acid from organic nitrogen substrates, particularly in the production of high-purity lactic acid, which is essential for the manufacturing of bioplastics and other industrial products (Thitiprasert et al., 2024). For example, the genome sequence analysis of Sporolactobacillus laevolacticus DSM442 has elucidated the mechanisms underlying its efficient production of D-lactic acid from organic nitrogen substrates, thereby providing a theoretical basis for its application in industrial fermentation (Wang et al., 2013). Additionally, studies on Sporolactobacillus are mainly focused on its isolation and purification methods and acid and bile salt resistance, and the probiotic potential of Sporolactobacillus requires further studies. This review aims to provide a theoretical basis and positive insights into the development and utilization of the Sporolactobacillus genus in the future.

2 Genomic characteristics

2.1 General features and average nucleotide identity (ANI) values of Sporolactobacillus

The rapid development of next-generation sequencing technology has led to a new understanding of the whole genome of a wide range of bacteria (Kamada et al., 2014), mainly because of the wide application of bioinformatics to analyze bacterial genomic information, shifting the direction of research from phenotype analysis to genome prediction. Compared with other well-known probiotics (such as Bifidobacterium and Lactobacillus), Sporolactobacillus has only been isolated from a few samples; therefore, the genomic novelty of Sporolactobacillus is limited. According to the National Center for Biotechnology Information (NCBI) database, as of May 1, 2023, 11 species and 20 strains of the genus Sporolactobacillus have been identified. Of these 20 Sporolactobacillus strains, 35 % of the strains were from unknown sources, 35% were isolated from soil and tree barks, three from fermented food, one was from spoiled food, and the remaining one strain of S. inulinus was isolated from chicken feed. Detailed information on the genomes of all 20 strains is presented in Table 1. The genome sizes of most Sporolactobacillus strains range from 2.87 Mb to 4.46 Mb (median genome size = 3.48 Mb). The genome size within the same genus varies significantly, which may be attributed to different functions such as translation, ribosomal structure and biogenesis, and DNA replication, recombination, and repair. These categories show a strong correlation with genome size (Konstantinidis and Tiedje, 2004). Additionally, as shown in Fig. 2, strains with smaller genomes also have fewer unique genes. Corresponding studies indicate that species with larger genomes may dominate in environments that are resource-scarce but diverse and slow-growing (Frank et al., 2002). For example, the species with the largest genome, Sporolactobacillus shoreicorticis, was isolated from tree bark. Sporolactobacillus has a stable guanine and cytosine content (GC content), ranging from 41.90% to 49.50% (median GC content = 45.10%), and a median protein count of 3171.Table 1 Genomic characteristics of Sporolactobacillus species and strain types.

Table 1Species	Number of Genomes	Total Length (Mb)	Median GC%	Median Protein Count	
Sporolactobacillus terrae	7	3.29	45.30	3070	
Sporolactobacillus laevolacticus	3	3.60	42.70	3410	
Sporolactobacillus vineae	2	2.87	49.50	2671	
Sporolactobacillus inulinus	3	3.07	45.10	2767	
Sporolactobacillus pectinivorans	1	3.93	44.30	3604	
Sporolactobacillus shoreicorticis	1	4.46	43.20	4275	
Sporolactobacillus kofuensis	1	2.96	41.90	2728	
Sporolactobacillus spathodeae	1	2.90	45.20	2545	
Sporolactobacillus putidus	1	3.48	46.60	3171	
Sporolactobacillus shoreae	1	3.65	45.30	3501	
Sporolactobacillus nakayamae	1	3.54	43.80	3308	

Average Nucleotide Identity (ANI) is defined as the base-level similarity between homologous genomic fragments of two microbial genomes. It is distinguished by its high discriminatory power among closely related species. ANI serves as an alternative to DNA-DNA hybridization (DDH), with the optimal species boundary threshold recommended to be between 95 and 96% (Lindsey et al., 2023). And the pairwise ANI values of the Sporolactobacillus genome ranged from 69.36% to 100% (Fig. 1), suggesting that significant genetic differences between species within the genus Sporolactobacillus. Based on the pairwise ANI analysis results, the ANI values between species within the genus Sporolactobacillus range from 69.36% to 93.84%, while the values between strains within the same species are all above 95–96%. This indicates significant genetic differences between species within the genus Sporolactobacillus, but relatively small differences between strains within the same species (Ciufo et al., 2018).Fig. 1 Pairwise average nucleotide identity(ANI) values of 20 Sporolactobacillus strains.

Fig. 1

Fig. 2 (A) Pan-genome and core genes of 20 Sporolactobacillus strains. (B) Venn diagram displaying core genes and unique genes of Sporolactobacillus strains.

Fig. 2

2.2 Pan-genome and core genome of Sporolactobacillus

Pan-genome is defined as the assembly of all genetic information of a bacterium, encompassing both core and strain-specific genes, which reflect the species diversity among the strains (Liu et al., 2021). The genomes of 20 Sporolactobacillus strains submitted to NCBI have been analyzed regarding their pan-genome and core genes, and the total number of genes and strain-specific genes of all 20 strains were determined (Fig. 2A). The pan-genome of all 20 Sporolactobacillus strains consists of 10963 genes, and the pan-genome curve tends to increase with the inclusion of additional Sporolactobacillus genomes, indicating the presence of an open pan-genome. In contrast, the curve for the core genome is progressively clustered, suggesting that the 983 genes that constitute approximately 8.23% of the entire genome are highly similar and can be representative of the genus Sporolactobacillus as a whole. The number of strain-specific genes in each strain varied from 11 to 605, with Sporolactobacillus shoreicorticis LMG 29111 possessing the highest number of unique genes (Fig. 2B). This may be attributed to its median protein count and total length (Table 1). Moreover, the bacteriocin distribution analysis reveals that this strain harbors the highest number of bacteriocin operons among all Sporolactobacillus strains examined. Isolated from tree bark in Thailand, the unique genetic features of this strain confer enhanced adaptability to the harsh ecological environment. Additionally, enzyme activity assays demonstrate that this strain exhibits significantly higher α, β-galactosidase activity compared to other related Sporolactobacillus strains, suggesting it may be the only strain within the genus with the potential to utilize lactose (Tolieng et al., 2017).

2.3 Phylogenetic analysis of Sporolactobacillus

Comparative genomic analyses of 20 Sporolactobacillus strains and constructed phylogenetic tree show the variability among different Sporolactobacillus species and their evolution path (Fig. 3). The phylogenetic tree indicates that Sporolactobacillus formed a paraphyletic cluster, suggesting that all the strains traced their origins back to a common ancestral progenitor, showcasing their shared lineage. Based on different evolutionary relationships, Sporolactobacillus primarily exists in two evolutionary branches. The 20 strains of Sporolactobacillus can be divided into 4 distinct clusters. Except for Sporolactobacillus spathodeae DSM100968, which is in one cluster, the other strains are divided into 6 smaller clusters, each containing 2–7 individual strains. For example, all the Sporolactobacillus terrae strains are in one cluster, confirming that these 7 strains belong to the same species. Meanwhile, through the phylogenetic tree, we found that Sporolactobacillus strains from the same ecological niche do not exist in the same branch, which may indicate that the phylogenetic evolution of Sporolactobacillus is not related to their isolation sources.Fig. 3 Phylogenetic tree of 20 Sporolactobacillus strains based on 16S ribosomal RNA gene sequences.

Fig. 3

2.4 Carbohydrate metabolism and genotype analyses

Previous studies have shown that some strains of Sporolactobacillus can use the host-derived glycans for metabolism. Basic local alignment search tool analysis was performed on 20 Sporolactobacillus strains to determine if this carbohydrate metabolic capacity exists across the genus. To validate the genotype and phenotype of Sporolactobacillus strains, host- and plant-derived sugars and different carbon sources have been tested. For example, Sporolactobacillus pectinivorans GD201205 produces acid from D-glucose, D-fructose, D-mannose, sucrose, raffinose, and turanose, but not from glycerol, erythritol, D-arabinose, and L-arabinose (Lan et al., 2016). And species isolated by Kitahara from the chicken feed was named S. inulinus because it produced lactic acid by fermenting inulin (Kitahara and Suzuki, 1963).

Prediction of carbohydrate-active enzymes (CAZymes) for the genomes of 20 Sporolactobacillus strains (Fig. 4), to verify the degree of utilization of different carbohydrates by different Sporolactobacillus strains, has identified 112 CAZymes for Sporolactobacillus species, including 4 Auxiliary Activities(AAs), 20 Carbohydrate-Binding Modules(CBMs), 10 Carbohydrate Esterase(CEs), 56 Glycoside Hydrolases (GHs), 20 Glycosyl Transferases (GTs), and 5 Polysaccharide Lyases(PLs). Notably, GT2, GT4, and CBM50 are present in all strains in relatively high content, and S. shoreicorticis LMG29111 possesses most enzymes (up to 182), whereas S. inulinus NBRC111894 possesses least variety of enzymes (64).Fig. 4 Carbohydrate metabolic capacity of Sporolactobacillus.

Fig. 4

GTs are involved in carbohydrate synthesis. Usually, CAZymes increase the catalytic activity of associated CAZymes, but they do not possess catalytic activity. The evolution and acquisition of specific CAZymes may provide a competitive advantage for some bacteria, such as human intestinal bacteria, with a large part of their genome dedicated to CAZymes. GHs compose the largest class of CAZymes and are primarily responsible for carbohydrate degradation; they are the most extensively studied CAZymes (Wardman et al., 2022).

2.5 Distribution of bacteriocin operons in Sporolactobacillus

Bacteriocin is a peptide produced by bacteria that can act as an antimicrobial agent to effectively inhibit the growth and reproduction of competing bacteria, thus, providing a growth advantage (Yadav et al., 2019). As shown in Fig. 5, we analyzed 20 strains of Sporolactobacillus. Sporolactobacillus species synthesizes 29 bacteriocins, including Sactipeptides, Lanthipetides, Paeninodian, Enterocin, Amylocylicin, UviB, Lactococcin, Closticin, and ZoocinA. However, the potential 13 operons that have been identified in Sporolactobacillus species seem to lack specific adenosine triphosphate ATP-binding cassette transporters, indicating apparent incompleteness.Fig. 5 Potential bacteriocin operons identified in 11 Sporolactobacillus species.

Fig. 5

3 Distribution and pure culture methods

Sporolactobacillus has been isolated from chicken feed, the rhizosphere of wild plants (Yanoshi, 1967), soil (Chang et al., 2008), anaerobic cattle waste digester (Sharma and Hobson, 1986), Nile River water (Ammar et al., 1986), and Japanese pickles (Chiou et al., 2019). Additionally, small amounts of bacteria have been reported in herbivore feces, cattle rumen, and final waste from slaughterhouses. Although some strains of Sporolactobacillus can be isolated from other habitats, they are present in small quantities in food and the environment. For example, Doores and Westhoff (Doores and Westhoff, 1983) used a selective method to obtain the gene of Sporolactobacilli, and of the 699 samples examined, two strains of Sporolactobacillus were isolated, both from soil samples.

Sporolactobacillus genes belong to the family Lactobacillaceae; however, they do not have the same strict dietary requirements as other lactobacilli, making their isolation and culture in anaerobic or microaerophilic environments easier (Sharma, 1992).

Distribution and pure culture methods of Sporolactobacillus are shown in Table 2. Kitahara and Suzuki used a straightforward medium with 2% glucose, 0.5% yeast extract, and 0.5% peptone (GYP medium) (Kitahara and Suzuki, 1963). The cultures were then incubated at 30 °C or 37 °C. Furthermore, the inclusion of a small quantity of water-insoluble calcium carbonate in the medium contributed to the initial selection process. Because of the acid released from growing colonies, a clear halo was produced, indicating the presence of Sporolactobacillus. With continuing research on Sporolactobacillus selection, the selection medium for Sporolactobacillus has been optimized. In later studies, water-soluble salts have been added to the original medium, with the pH adjusted to 6.8 (Lan et al., 2016; Fujita et al., 2010). Most strains of Sporolactobacillus grow well in both Lactobacillus media (namely deMan Rogosa Sharpe [MRS] and ATP media); however, GYP medium is more suitable for culturing Sporolactobacillus and has been formally validated to isolate other Bacillus species (Doores and Westhoff, 1983). Studies suggest that the samples to be isolated should be enriched by inoculating them after homogenization in the Sporolactobacillus medium (Sharma and Hobson, 1985) and that the entire isolation process should always be performed under anaerobic conditions. A selective screening protocol was investigated, in which Sporolactobacillus was enriched in various samples using a modified Lactobacillus MRS medium before isolation and screening. Glucose was replaced with α-methyl glucoside, potassium sorbate was added as a mold inhibitor (Botha and Holzapfel, 1987), bromocresol green was used as an acid-producing indicator, and the medium was adjusted to pH 5.5 using acetic acid (Doores and Westhoff, 1983).Table 2 Isolation sources of Sporolactobacillus reported in the literature.

Table 2Species	Isolation sources	Pure culture medium	Colony characteristics	References	
Sporolactobacillus inulinus	Chicken feed food	GYP medium	Grayish white pin-point colonies	Kitahara and Suzuki (1963)	
Sporolactobacillus laevolacticus	Compost pile	CYC medium	Round, obscure-edged, translucent, and cream-colored colonies	Hatayama et al. (2006)	
Sporolactobacillus vineae	Vineyard soil	GYP medium	Round, smooth, and ivory-white colonies	Chang et al. (2008)	
Sporolactobacillus putidus	Spoiled orange juice	PCA medium	Flat, smooth, and creamy-white colonies	Fujita et al. (2010)	
Sporolactobacillus shoreaeSporolactobacillus spathodeae	Tree barks in Thailand	–	–	Thamacharoensuk et al. (2015)	
Sporolactobacillus pectinivorans	Spoiled jelly	Modified GYP medium	Circular, flat, and opaque-white colonies	Lan et al. (2016)	
Sporolactobacillus shoreicorticis	Tree bark	0.5% CaCO3 GYP medium	Circular and smooth-white colonies	Tolieng et al. (2017)	
Sporolactobacillus nakayamae, Sporolactobacillus terrae, Sporolactobacillus kofuensis, Sporolactobacillus inulinus	Tree barks in Thailand	GYP medium	Circular, smooth, and white-colored colonies	Thamacharoensuk et al. (2017)	
Sporolactobacillus inulinus	Kôso, a Japanese Sugar–vegetable fermented beverage	GY medium	Circular, smooth-edged, and white-colored colonies	Chiou et al. (2019)	
Sporolactobacillus nakayamae	Northeastern Chinese soybean paste	–	–	Ling et al. (2022)	
GYP, glucose–yeast extract–peptone; GY, glucose–yeast extract; PCA, plate count agar; and CYC, Czapek-Dox-yeast extract-Bacto vitamin assay Casamino acids.

4 Morphological and physiological characteristics

4.1 Morphological characteristics

Sporolactobacillus typically occurs individually or in pairs. Its cells are rod-shaped but rarely form short chains, which can be formed in both aerobic and anaerobic cultures. However, Sporolactobacillus does not differ from other typical LAB regarding endospore production, which is usually within or at the end of the chain, and the presence of a periplasmic flagellum capable of locomotion (Sharma, 1992). It produces D-lactic acid via homotypic fermentation of the sugar, but it does not produce oxidase enzymes. The ideal temperature for the growth of Sporolactobacillus is 35 °C.

4.2 Physiological characteristics

To become a probiotic, Sporolactobacillus must meet several conditions, the most basic of which is its acid and bile salt tolerance, ability to adhere to the mucous membranes of the intestinal epithelia, colonization of the flora ecosystem to resist harmful organisms, and secretion of antimicrobial substances (Huang et al., 2007). The spores of Sporolactobacillus are resistant to unfavorable intestinal conditions and can survive in the intestine, providing probiotic benefits to the host.

4.2.1 Acid and bile salt resistance

Probiotics can play their role in the human body only if the bacteria passes through the stomach and small intestine with certain activity and colonizes the colon; survival of probiotics and their colonization in the human body is mainly related to their ability to tolerate acid and bile salts. Studies on spore-forming LAB (SFLAB) (Hyronimus et al., 2000) reveal that many factors make SFLAB good candidates for probiotic use, such as bulk culturing, organic acid production, and sporulation ability.

S. inulinus BCRC14647 was shown to exhibit better physiological properties than two strains of Bifidobacterium bifidum (Huang et al., 2007), which are widely used probiotics. S. inulinus BCRC14647 has shown a much higher survival rate in the acid tolerance test and more viability in the bile salt tolerance test than those of the two reference strains under the same treatment conditions (Huang et al., 2007). Hence, S. inulinus has high acid tolerance and can effortlessly traverse the small intestine and stomach, without losing its activity after reaching the action site in the large intestine. In vitro experiments on acid and bile salt tolerance have shown that Sporolactobacillus has great potential to colonize the host. Similarly, Hyronimus et al. have also demonstrated the acid- and bile salt-tolerance of Sporolactobacillus (Hyronimus et al., 2000). Compared to other spore-forming bacteria, Sporolactobacillus laevolacticus exhibited a very high survival rate after treatment at pH 3, but showed weaker tolerance to 0.3% bile. These results preliminarily indicate that not all strains within the Sporolactobacillus genus possess both acid and bile tolerance properties. Moreover, if Sporolactobacillus is to be considered a promising probiotic candidate, further confirmation of other parameters is necessary (Salminen et al., 1996).

4.2.2 Antibacterial properties

Sporolactobacillus can produce lactic acid via homotypic fermentation, along with hydrogen peroxide, both of which are pathogenic-bacteria-inhibiting metabolites.

Sporolactobacillus can produce some bacteriocins; thus, it can exhibit some antibacterial activity. Most of the bacteriocins produced by Sporolactobacillus exert some inhibitory effect on gram-positive bacteria with similar relatives, whereas lactic acid has a broader inhibitory range (Murinda et al., 1995). Novel bacteriocins produced by Sporolactobacillus are useful in the modern food industry. Current research indicates that Sporolactobacillus and other halophilic bacteria exhibit unique enzyme activities in extreme environments (Harirchi et al., 2022). These studies indirectly suggest the potential functionality of Sporolactobacillus in mitigating the effects in halophilic foods.

Sporolactobacillus exhibits characteristics of Bacillus and Lactobacillus. Hence, these non-traditional SFLAB have potential antibacterial effects. Sporolactobacillus exhibits some anti-Listeria monocytogenes properties and an inhibition circle when cultured on an agar medium (Murinda et al., 1995).

4.2.3 Heat resistance

Sporolactobacillus exhibits different thermal properties in different culture media. The composition of the culture medium affects the capacity of Sporolactobacillus to resist heat resistance (Mafart and Leguérinel, 1997). For example, carbohydrate, one of the medium components, is a very important factor, and the presence of sucrose makes the apparent heat resistance of Sporolactobacillus weaker than that by glucose, possibly because of the higher molecular weight of sucrose, which slows the overall rate of its entry into the cell. Furthermore, the cellular utilization of sucrose makes the osmotic pressure gradient across the cell membrane extremely imbalanced, leading to a decrease in the cell survival rate (Coroller et al., 2001).

In the genus Sporolactobacillus, S. inulinus is the only species for which the thermal inactivation data have been published. In Bacillus agar with 2% α-methylglucoside, S. inulinus exhibited the highest degree of heat resistance. Additionally, a study (Bozkurt et al., 2016) used a circulating water bath to test the heat resistance phenotype of Sporolactobacillus nakayamae and showed that the growth conditions and medium composition used for spore counting following heat treatment were the primary determinants of the heat resistance phenotype of the strain.

5 Applications

Sporolactobacillus exhibits excellent LAB characteristics and can ferment and decompose glucose to produce lactic acid, phenyllactic acid (PLA), and polylactic acid via polymerization of D-lactic acid with high optical purity (Zhang et al., 2022). Regarding production, lactic acid, PLA, and polylactic acid have great application value. With the increased range of isolated strains and the discovery of their related physiological and biochemical properties, studies on the applications of Sporolactobacillus have gradually increased in recent years.

Additionally, the economic significance of lactobacilli probably increases the relevance of Sporolactobacillus. However, there is insufficient direct data to support this; therefore, further studies are needed (Sharma, 1992). The physiological characteristics and specialized metabolites of many Bacillus species have been extensively utilized in the pharmaceutical, agricultural, and food industries. Bacillus species are particularly valued for their ability to produce antibiotics, enzymes, and probiotics (Ray et al., 2014). These applications suggest that Sporolactobacillus, which exhibits similar characteristics, may also possess significant economic potential. Furthermore, Sporolactobacillus has demonstrated the capability to efficiently produce D-lactic acid from organic nitrogen substrates, highlighting its potential applications in biotechnology and industrial fermentation, especially in the production of high-purity lactic acid. This is crucial for the manufacturing of bioplastics and other industrial products (Thitiprasert et al., 2024). Additionally, recent discoveries provide valuable insights into the metabolic pathways and enzyme activities of Sporolactobacillus, further supporting its potential in industrial fermentation applications (Wu et al., 2019a).

5.1 Lactic acid production

Sporolactobacillus does not have a high nutritional requirement as other LAB, which makes the use of Sporolactobacillus highly economical in lactic acid production. Sporolactobacillus metabolizes carbohydrates to produce lactic acid, which is a beneficial organic acid with a wide range of applications (Wee et al., 2006).

Sporolactobacillus preferentially uses the fermentation rather than the tricarboxylic acid (TCA) cycle to produce lactic acid. Owing to homologous fermentation, Sporolactobacillus produces lactic acid with high optical purity, enabling the application of this method for large-scale industrial production. For example, S. inulinus YBS1-5 is a high-optical-purity D-lactate-producing strain (Wu et al., 2019a), which is attributed to its three potential D-lactate dehydrogenases (LDHs) and two putative L-LDHs, which are produced by Escherichia coli using various neutralizing agents after being cloned, yielding experimental results that may provide a strong reference for further improvement of strain performance and polymeric grade D-lactate (Wu et al., 2019b).

Neutralizing agents are essential for cell growth and D-lactate production and purification during the fermentation process (Zheng et al., 2017a). The most frequently used neutralizing agent in lactic acid fermentation is calcium carbonate (CaCO3), which neutralizes lactic acid very slowly, mildly, and at a low pH. However, the optimal pH for fermentation-induced lactic acid production in S. inulinus is higher; therefore, fermentation with neutralizing agents such as NaOH or KOH at a high pH increases the yield, productivity, and optical purity of lactic acid. Therefore, an acidic environment may not be conducive to LDH activity (Zheng et al., 2017b).

5.1.1 Lactic acid production using inexpensive nitrogen sources

It is necessary to improve the optical purity of lactic acid and reduce the production cost. During homozygous lactic acid fermentation in Sporolactobacillus, the nitrogen source is the main cost-related factor. There are various nitrogen sources available in the market, among which yeast extract is the best choice for lactic acid production by microorganisms because of its richness in amino acids and mineral salts. However, the biggest disadvantage of yeast extract is its high cost, which limits its use in large-scale industrial production. Additionally, different strains of Sporolactobacillus exhibit different lactic acid production efficiencies with different nitrogen sources. In Sporolactobacillus hominis, yeast extract is the nitrogen source in the biosynthetic fermentation medium for lactic acid production, which is expensive and unsuitable for large-scale industrial production. Therefore, identifying an inexpensive alternative source of nitrogen for economical, large-scale fermentation to produce lactic acid is important (Fan et al., 2017).

S. inulinus is considered the best strain for D-lactate production (Thitiprasert et al., 2021). S. inulinus ATCC 15538 has been shown to produce PLA (2-hydroxy-3-phenylpropanoic acid) via whole-cell biotransformation (Cheng et al., 2022). LDH produced by S. inulinus ATCC 15538 can reduce the amount of phenylpyruvate and accelerate the production of PLA; the produced LDH exhibits a highly specific and efficient D-LDH activity. Reportedly, S. inulinus ATCC 15538 has shown good performance in D-PLA production with a fast conversion rate and high conversion yield. Sporolactobacillus terrae has also shown a high fermentation capacity for the sustained production of D-lactic acid using agroindustrial wastes (such as peanut, soybean, and corn syrup meals) (Han et al., 2019).

During the hydrolysis of a nitrogen source by S. inulinus, almost all residues were hydrolyzed and lactic acid was produced (Zheng et al., 2014). The efficiency of lactic acid production by S. inulinus fermentation is not determined by the type of agriculture but by the final degree of hydrolysis. The degradation of nitrogen-rich agriculture in the absence of a more efficient hydrolysis method is the chemical method. Brock examined how different chemicals and enzymatic techniques affected the ability of S. inulinus to produce lactic acid and breakdown protein-rich agricultural wastes and found that hydrolysis of many agricultural straws (such as rapeseed meal, sunflower meal, wheat gluten, and corn gluten) with 3 M H2SO4 was an effective alternative to yeast dip (Brock et al., 2019). Furthermore, it was found that Sporolactobacillus laevolacticus DSM442 can replace the consumption of expensive yeast dip by LAB, as it can produce D-PLA owing to its low nutritional requirements during fermentation (Lan et al., 2016). When pea seeds were hydrolyzed with protein hydrolase as a nitrogen source for lactic acid fermentation, S. laevolacticus DSM442 produced slightly lower D-PLA than that with yeast dip, but the optical purity of the lactic acid was essentially the same as that obtained using yeast dip.

5.1.2 Lactic acid production using inexpensive carbon sources

In homolactic fermentation by Sporolactobacillus, glucose is the carbon source for producing lactic acid, but the cost of glucose is high. Promoting large-scale industrial synthesis of chemicals using agriculture-based feedstocks as the carbon source can greatly reduce production costs. Presently, many studies have focused on L-lactic acid production from renewable resources, but only a few have focused on large-scale fermentation for D-lactic acid production (Liang and Wan, 2015).

A recent study showed that Sporolactobacillus can use cassava fiber waste (CFW) as a carbon source for fermentation, which not only reduces the production cost but also improves the optical purity of lactic acid. Lactic acid produced from the enzymatic digestion of CFW, an inexpensive alternative carbon source, was satisfactory, and the S. inulinus strain was fully utilized to reduce the cost of the carbon source (Gali et al., 2021). The LAB strain showed no growth with acid-digested CFW, indicating the presence of inhibitory byproducts during fermentation, such as furfural and its derivatives. Compared with genetically engineered Bacillus subtilis strains that produced D-lactate with 98% optical purity, S. inulinus has yielded D-lactate (0.96 g/g) with 99.5% optical purity using CFW as the alternate carbon source under controlled laboratory operating conditions. The economic viability of raw materials used in lactic acid production is one of the greatest challenges (Swetha et al., 2023a, Swetha et al., 2023b). Due to the easily fermentable carbon sources in food waste, Sporolactobacillus can also utilize food waste to produce lactic acid, achieving a maximum lactic acid concentration of 58 g/L and a maximum yield of 96.7% (RedCorn and Engelberth, 2016). Moreover, a suitable method has now been developed to produce pure lactic acid from food waste, achieving a lactic acid purity of up to 100% (Li et al., 2015a, Li et al., 2015b).

5.2 Phenyllactic acid production

2-hydroxy-3-phenylpropanoic acid（PLA）is a phenolic acid phytochemical with antibacterial activity (Li et al., 2015a, Li et al., 2015b) and is mainly formed by Lactobacillus during phenylalanine and central carbon metabolism (Rajanikar et al., 2021). PLA was originally detected in honey and sourdough (Isidorov et al., 2015). Recently, PLA was also found in traditional Chinese pickles (Li et al., 2015a, Li et al., 2015b), and it was found that high concentrations of lactic acid can react with polylactic acid to protect pickles from deterioration. The pathway of PLA production is shown in Fig. 6.Fig. 6 Phenyllactic acid production pathway.

Fig. 6

Among the stereoisomers of polylactic acid, D-PLA exhibits better antibacterial and immunomodulatory activities than those of L-PLA (Mu et al., 2012). At the genetic level, Sporolactobacillus possesses a highly active D-LDH gene, which is possibly encoded by Sporolactobacillus for the effective transformation of D-PLA (Sakurai et al., 2021).

PLA is a broad-spectrum antibacterial substance (Siedler et al., 2019) and has no side effects on human health (F. Liu et al., 2020). PLA exhibits strong anti-corruption activity against yeast, bacteria, and molds, inducing cell membrane breaks and biofilm formation (Chatterjee et al., 2017). Synthetic medications are often used to treat illnesses; however, they have major adverse effects. PLA can be used as a new-generation drug for the treatment of various diseases, primarily because it is a natural compound that does not cause adverse reactions. PLA can relieve Salmonella typhimurium-induced colitis by regulating intestinal flora and eliminating inflammation, considerably increasing the concentration of short-chain fatty acids (Zhou et al., 2021). Additionally, PLA may be a candidate drug for preventing type 2 diabetes by promoting adipocyte development and glucose consumption (Ilavenil et al., 2015). PLA may also be a potential regulator of human immunity (Peters et al., 2019). Therefore, PLA produced by metabolizing carbohydrates is likely to serve as a next-generation probiotic to alleviate human diseases.

5.3 Polylactic acid production

The monomeric unit of polylactic acid, namely polylactic acid, is produced by biological fermentation, and these are not only environmentally friendly but also reduce the wastage of non-renewable resources (Swetha et al., 2023a, Swetha et al., 2023b). Polylactic acid has a high mechanical strength, making it an alternative to non-degradable, oil-based polymers. Polylactic acid has been listed as generally recognized as safe (GRAS) by the United States Food and Drug Administration (FDA) (Swetha et al., 2023a, Swetha et al., 2023b).

Polylactic acid is a new biodegradable plastic material. Presently, most studies are focused on its films for food preservation, biomedicine, and compound modification. Polylactic acid has an annual production of approximately 140,000 tons, and it is the most common biopolymer in the food packaging sector (Swetha et al., 2023a, Swetha et al., 2023b); studies have reported that polylactic acid is safe and harmless as a food packaging material.

5.4 Biological hydrogen production

Dark fermentation is the most commonly used method for biological hydrogen production. Dark fermentation has many advantages, for example, it is environment friendly and can replace traditional coal-based hydrogen production (Das, 2001). However, the dark fermentation method for biological hydrogen production has certain limitations, such as insufficient conversion of substrate consumed and production of undesirable byproducts, which eventually reduce the actual hydrogen production compared to the theoretical yield (Kim et al., 2021).

Present studies have shown that the performance of organisms in hydrogen production is closely related to the parameters of acid-producing fermentation and that important products in the acid-producing biochemical pathway are converted into hydrogen by different microbial communities. A study showed that the genus Sporolactobacillus is a main mixed culture for hydrogen production under batch conditions (Park et al., 2021) and elucidated the synergistic interaction between Clostridium and LAB using the identified strains. Moreover, Clostridium butyricum and Sporolactobacillus vineae can produce lactic acid when co-cultured, which can be further converted to butyric or acetic acid and hydrogen.

Associating the operating conditions of dynamic membrane bioreactors (DMBRs) to changes in microbial communities can help assess stable biohydrogen production methods (Kim et al., 2021). Reportedly, at a relatively low substrate concentration, the abundance of Sporolactobacillus species increases, which negatively affects hydrogen production; thus, when operating the DMBR, an appropriate substrate concentration needs to be maintained to achieve a high hydrogen production rate.

5.5 Livestock application in feed

China is a large agricultural country with increasing industrialization and intensification of livestock and poultry. Owing to the strict restrictions on antibiotics, livestock farming has become more challenging in China. The incorporation of probiotics in animal feed can serve as a substitute for antibiotics, thereby enhancing the safety of animal use and treating bacterial infections (Soares et al., 2023). Furthermore, probiotics can more effectively manage the morbidity and mortality associated with intestinal infections, consequently improving animal growth and feed efficiency (Carlin et al., 2010).

Direct-fed microorganisms (DFM) are now one of the main alternatives to antibiotics in the livestock industry (Ban and Guan, 2021). Probiotics, being the major DFM, are added directly as feed supplements to affect the balance of gut microorganisms in livestock (Hill, 1993). Probiotics have been reported to improve feed utilization, accelerate overall growth, and increase milk and egg production (Hyronimus et al., 2000) by improving the general health of cattle, pigs, and chickens; they can also be applied in aquaculture by increasing the tolerance of fish to acute stress (Rollo et al., 2006). For ruminants, the main focus is on improving the digestive system to improve their ability to prevent disease (Azzaz et al., 2015) and increase cow productivity (Goetz et al., 2021). There are many probiotics for animals, including Lactobacillus, Bifidobacterium, Pediococcus, and some yeasts (Hill, 1993). There have been some studies utilizing probiotics to alleviate symptoms of gastrointestinal diseases in animals. For example, research on the growth performance, nutrient digestion, and gut microbiota of weaning piglets has shown that the addition of probiotics can lead to greater weight gain, higher protein digestibility, and enhanced immune system function (Mun et al., 2021).

Spore-forming bacteria have received considerable attention in recent years due to their ability to produce spores, making them frequently used as probiotics in animal feed. The capability of spore-forming provides significant resistance to the heat involved in the production process and allows for extended storage times (Simon, 2005). Sporolactobacillus is an spore-forming bacteria, which can exist in the form of spores to improve stress resistance (such as at high temperatures), allowing large-scale production of ssprobiotic animal feed (Hyronimus et al., 2000).

6 Outlook

Probiotics have garnered increasing attention; however, the use of spore-forming microorganisms as probiotics has not been thoroughly explored. The exploration of these strains as probiotics remains an intriguing avenue, primarily due to their increased resistance to adverse environmental conditions, making them particularly appealing for commercial applications in animal husbandry (Elshaghabee et al., 2017). The key advantages of sporeformers as probiotics are their ease of production and remarkable stability in the final products.

In contrast to extensively studied probiotics such as Lactobacillus and Bifidobacterium, sporeformers present a unique characteristic, that is, their spores are highly resistant to digestion and absorption by the body, thereby necessitating further investigation of their direct probiotic effects on the body (Sanders et al., 2003) and safety concerns regarding oral administration of large amounts of non-gastrointestinal (GI) live microorganisms.

The mechanism of sporeformers as probiotics remains unknown, in addition to their safety and the germination of their budding spores in the GI tract and the subsequent survival of the corresponding nutrient cells, which mainly includes the metabolites of microoranisms, the secretion of bacteriostatic agents, and immunomodulatory effects. The future potential of Sporolactobacillus as a probiotic requires accurate identification and characterization. Evaluating its antagonistic activity against potential pathogenic microorganisms is also a standard for assessing whether a strain has probiotic potential (Sorokulova, 2008).

Although the application of Sporolactobacillus as a probiotic has not been thoroughly investigated, it offers several advantages. These include the ability to homotypically ferment whole cells for lactic acid production under relatively mature conditions. Moreover, its betas production can withstand harsh industrial processing environments. The ability to produce spores enables Sporolactobacillus to withstand the high temperatures during feed production and ensures the viability of the probiotics. The stability of the spores allows for extended storage periods without losing efficacy. Additionally, Sporolactobacillus can serve as a natural alternative to antibiotics, promoting animal health and growth. Thus, altogether, Sporolactobacillus shows great potential to be included in the list of edible strains as probiotics.

Funding information

This work was supported by 10.13039/501100001809 National Natural Science Foundation of China (U23A20261 ), 10.13039/501100004608 Natural Science Foundation of Jiangsu Province (BK20220155 ) and 10.13039/501100001809 National Natural Science Foundation of China (32372296 ).

CRediT authorship contribution statement

Xinyu Guo: Conceptualization, Data curation, Investigation, Methodology, Writing – original draft, Writing – review & editing. Leilei Yu: Conceptualization, Funding acquisition, Supervision. Meifang Xiao: Conceptualization. Xiaojie Zang: Conceptualization, Data curation, Writing – review & editing. Chengcheng Zhang: Conceptualization. Arjan Narbad: Conceptualization, Validation. Wei Chen: Conceptualization. Fengwei Tian: Conceptualization. Qixiao Zhai: Conceptualization.

Declaration of competing interest

All the authors of this review have approved the manuscript that is enclosed and no conflict of interest exists in the submission of this manuscript, and the contents of this manuscript have not copyrighted or published previously and is not under consideration for publication elsewhere.

Data availability

Data will be made available on request.
==== Refs
References

Alexandri M. Schneider R. Mehlmann K. Venus J. Recent advances in d-lactic acid production from renewable resources: case studies on agro-industrial waste streams Food Technol. Biotechnol. 57 2019 293 304 10.17113/ftb.57.03.19.6023 31866743
Ammar M.S. Elwan S.H. Razak A.A. Ghanem E.H. Seasonal changes of bacterial counts and bacterial species in Nile River water at two water purification stations in Cairo Jpn. J. Limnol. 47 1986 109 114 10.3739/rikusui.47.109
Azzaz H.H. Morsy T.A. Murad H.A. Microbial feed supplements for ruminant's performance enhancement Asian J. of Agricultural Research 10 2015 1 14 10.3923/ajar.2016.1.14
Ban Y. Guan L.L. Implication and challenges of direct-fed microbial supplementation to improve ruminant production and health J. Anim. Sci. Biotechnol. 12 2021 109 10.1186/s40104-021-00630-x 34635155
Botha S.J. Holzapfel W.H. Resistance of Sporolactobacillus to potassium sorbate and sodium nitrite Int. J. Food Microbiol. 5 1987 331 336 10.1016/0168-1605(87)90047-X
Bozkurt H. David J.R.D. Talley R.J. Lineback D.S. Davidson P.M. Thermal inactivation kinetics of sporolactobacillus nakayamae spores, a spoilage bacterium isolated from a model mashed potato–scallion mixture J. Food Protect. 79 2016 1482 1489 10.4315/0362-028X.JFP-16-103
Brock S. Kuenz A. Prüße U. Impact of hydrolysis methods on the utilization of agricultural residues as nutrient source for D-lactic acid production by sporolactobacillus inulinus Fermentation 5 2019 12 10.3390/fermentation5010012
Carlin F. Brillard J. Broussolle V. Clavel T. Duport C. Jobin M. Guinebretière M.-H. Auger S. Sorokine A. Nguyen-Thé C. Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment Food Res. Int. 43 2010 1885 1894 10.1016/j.foodres.2009.10.024
Chang Y.-H. Jung M.Y. Park I.-S. Oh H.-M. Sporolactobacillus vineae sp. nov., a spore-forming lactic acid bacterium isolated from vineyard soil Int. J. Syst. Evol. Microbiol. 58 2008 2316 2320 10.1099/ijs.0.65608-0 18842848
Chatterjee M. D'Morris S. Paul V. Warrier S. Vasudevan A.K. Vanuopadath M. Nair S.S. Paul-Prasanth B. Mohan C.G. Biswas R. Mechanistic understanding of Phenyllactic acid mediated inhibition of quorum sensing and biofilm development in Pseudomonas aeruginosa Appl. Microbiol. Biotechnol. 101 2017 8223 8236 10.1007/s00253-017-8546-4 28983655
Cheng Y. Park T.H. Seong H. Kim T. Han N.S. Biological characterization of D‐lactate dehydrogenase responsible for high‐yield production of D‐phenyllactic acid in Sporolactobacillus inulinus Microb. Biotechnol. 15 2022 2717 2729 10.1111/1751-7915.14125 35921426
Chiou T.-Y. Suda W. Oshima K. Hattori M. Matsuzaki C. Yamamoto K. Takahashi T. Draft genome sequence of sporolactobacillus inulinus NBRC 111894, isolated from kôso, a Japanese sugar-vegetable fermented beverage Microbiol Resour Announc 8 2019 e00751 10.1128/MRA.00751-19 19
Ciufo S. Kannan S. Sharma S. Badretdin A. Clark K. Turner S. Brover S. Schoch C.L. Kimchi A. DiCuccio M. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI Int. J. Syst. Evol. Microbiol. 68 2018 2386 2392 10.1099/ijsem.0.002809 29792589
Coroller L. Leguérinel I. Mafart P. Effect of water activities of heating and recovery media on apparent heat resistance of Bacillus cereus spores Appl. Environ. Microbiol. 67 2001 317 322 10.1128/AEM.67.1.317-322.2001 11133461
Das D. Hydrogen production by biological processes: a survey of literature Int. J. Hydrogen Energy 26 2001 13 28 10.1016/S0360-3199(00)00058-6
Dellaglio F. Bottazzi V. Vescovo M. Deoxyribonucleic acid homology among Lactobacillus species of the subgenus streptobacterium orla-jensen Int. J. Syst. Bacteriol. 25 1975 160 172 10.1099/00207713-25-2-160
Doores S. Westhoff D.C. Selective method for the isolation of Sporolactobacillus from food and environmental sources J. Appl. Bacteriol. 54 1983 273 280 10.1111/j.1365-2672.1983.tb02617.x 6853400
Duc L.H. Hong H.A. Barbosa T.M. Henriques A.O. Cutting S.M. Characterization of Bacillus probiotics available for human use Appl. Environ. Microbiol. 70 2004 2161 2171 10.1128/AEM.70.4.2161-2171.2004 15066809
Elshaghabee F.M.F. Rokana N. Gulhane R.D. Sharma C. Panwar H. Bacillus as potential probiotics: status, concerns, and future perspectives Front. Microbiol. 8 2017 10.3389/fmicb.2017.01490
Fan S. Breidt F. Price R. Pérez‐Díaz I. Survival and growth of probiotic lactic acid bacteria in refrigerated pickle products J. Food Sci. 82 2017 167 173 10.1111/1750-3841.13579 27984668
Fares C. Menga V. Martina A. Pellegrini N. Scazzina F. Torriani S. Nutritional profile and cooking quality of a new functional pasta naturally enriched in phenolic acids, added with β-glucan and Bacillus coagulans GBI-30, 6086 J. Cereal. Sci. 65 2015 260 266 10.1016/j.jcs.2015.07.017
Frank A.C. Amiri H. Andersson S.G.E. Genome deterioration: loss of repeated sequences and accumulation of junk DNA Genetica 115 2002 1 12 10.1023/a:1016064511533 12188042
Fujita R. Mochida K. Kato Y. Goto K. Sporolactobacillus putidus sp. nov., an endospore-forming lactic acid bacterium isolated from spoiled orange juice Int. J. Syst. Evol. Microbiol. 60 2010 1499 1503 10.1099/ijs.0.002048-0 19684317
Gali K.K. Reddy Tadi S.R. Mohan N. Swaminathan N. Katiyar V. Sivaprakasam S. Cost-effective valorization of cassava fibrous waste into enantiomerically pure D-lactic acid: process engineering and kinetic modelling approach Environ. Technol. Innov. 22 2021 101519 10.1016/j.eti.2021.101519
Goetz B.M. Lefler J. Abeyta M.A. Horst E.A. Mayorga E.J. Al-Qaisi M. Rodriguez-Jimenez S. Martino C. Izzo A. La R. Green H.B. Moore C.E. Embree M. Baumgard L.H. Effects of dietary microbial feed supplement on production efficacy in lactating dairy cows JDS Communications 2 2021 118 122 10.3168/jdsc.2020-0002 36339501
Han X. Huang K. Tang H. Ni J. Liu J. Xu P. Tao F. Steps toward high‐performance PLA: economical production of d ‐lactate enabled by a newly isolated sporolactobacillus terrae strain Biotechnol. J. 14 2019 1800656 10.1002/biot.201800656
Harirchi S. Sar T. Ramezani M. Aliyu H. Etemadifar Z. Nojoumi S.A. Yazdian F. Awasthi M.K. Taherzadeh M.J. Bacillales: from taxonomy to biotechnological and industrial perspectives Microorganisms 10 2022 10.3390/microorganisms10122355 Article 12
Hatayama K. Shoun H. Ueda Y. Nakamura A. Tuberibacillus calidus gen. nov., sp. nov., isolated from a compost pile and reclassification of Bacillus naganoensis Tomimura et al Int. J. Syst. Evol. Microbiol. 56 2006 2545 2551 10.1099/ijs.0.64303-0 1990 as Pullulanibacillus naganoensis gen. nov., comb. nov. and Bacillus laevolacticus Andersch et al. 1994 as Sporolactobacillus laevolacticus comb. nov 17082388
Hill M. Probiotics: the scientific basis Gut 34 1993 863 864
Huang H.-Y. Huang S.-Y. Chen P.-Y. King V.A.-E. Lin Y.-P. Tsen J.-H. Basic characteristics of Sporolactobacillus inulinus BCRC 14647 for potential probiotic properties Curr. Microbiol. 54 2007 396 404 10.1007/s00284-006-0496-5 17387552
Hyronimus B. Le Marrec C. Hadj Sassi A. Deschamps A. Acid and bile tolerance of spore-forming lactic acid bacteria Int. J. Food Microbiol. 61 2000 193 197 10.1016/S0168-1605(00)00366-4 11078170
Ilavenil S. Kim D. Valan Arasu M. Srigopalram S. Sivanesan R. Choi K. Phenyllactic acid from Lactobacillus plantarum PromotesAdipogenic activity in 3T3-L1 adipocyte via up-regulationof PPAR-γ2 Molecules 20 2015 15359 15373 10.3390/molecules200815359 26305241
Isidorov V.A. Bagan R. Bakier S. Swiecicka I. Chemical composition and antimicrobial activity of Polish herbhoneys Food Chem. 171 2015 84 88 10.1016/j.foodchem.2014.08.112 25308646
Islam S.U. Clinical uses of probiotics Medicine 95 2016 e2658 10.1097/MD.0000000000002658 26844491
Kamada M. Hase S. Sato K. Toyoda A. Fujiyama A. Sakakibara Y. Whole genome complete resequencing of Bacillus subtilis natto by combining long reads with high-quality short reads PLoS One 9 2014 e109999 10.1371/journal.pone.0109999
Keller D. Verbruggen S. Cash H. Farmer S. Venema K. Spores of Bacillus coagulans GBI-30, 6086 show high germination, survival and enzyme activity in a dynamic, computer-controlled in vitro model of the gastrointestinal tract Benef. Microbes 10 2019 77 87 10.3920/BM2018.0037 30694101
Kim D. Park J. Kim S. Kumar G. Lee B. Kumar S. Yoon J. Shift of microbial community structure by substrate level in dynamic membrane bioreactor for biohydrogen production Intl J of Energy Research 45 2021 17408 17416 10.1002/er.5737
Kitahara K. Lai C. On the spore formation of Sporolactobacillus inulinus J. Gen. Appl. Microbiol. 13 1967 197 203
Kitahara K. Suzuki J. Sporolactobacillus nov. subgen J. Gen. Appl. Microbiol. 9 1963 59 71 10.2323/jgam.9.59
Kitahara K. Toyota T. Auto-spheroplastization and cell-permeation in sporolactobacillus in Sporolactoballus inulinus J. Gen. Appl. Microbiol. 18 1972 99 107 10.2323/jgam.18.99
Konstantinidis K.T. Tiedje J.M. Trends between gene content and genome size in prokaryotic species with larger genomes Proc. Natl. Acad. Sci. USA 101 2004 3160 3165 10.1073/pnas.0308653100 14973198
Lan Q.X. Chen J. Lin L. Ye X.L. Yan Q.Y. Huang J.F. Liu C.C. Yang G.W. Sporolactobacillus pectinivorans sp. nov., an anaerobic bacterium isolated from spoiled jelly Int. J. Syst. Evol. Microbiol. 66 2016 4323 4328 10.1099/ijsem.0.001351 27516092
Li X. Chen Y. Zhao S. Chen H. Zheng X. Luo J. Liu Y. Efficient production of optically pure L-lactic acid from food waste at ambient temperature by regulating key enzyme activity Water Res. 70 2015 148 157 25528545
Li X. Ning Y. Liu D. Yan A. Wang Z. Wang S. Miao M. Zhu H. Jia Y. Metabolic mechanism of phenyllactic acid naturally occurring in Chinese pickles Food Chem. 186 2015 265 270 10.1016/j.foodchem.2015.01.145 25976820
Liang S. Wan C. Carboxylic acid production from brewer's spent grain via mixed culture fermentation Bioresour. Technol. 182 2015 179 183 10.1016/j.biortech.2015.01.082 25698409
Lindsey R.L. Gladney L.M. Huang A.D. Griswold T. Katz L.S. Dinsmore B.A. Im M.S. Kucerova Z. Smith P.A. Lane C. Carleton H.A. Rapid identification of enteric bacteria from whole genome sequences using average nucleotide identity metrics Front. Microbiol. 14 2023 10.3389/fmicb.2023.1225207
Ling H. Shi H. Chen X. Cheng K. Detection of the microbial diversity and flavour components of northeastern Chinese soybean paste during storage Food Chem. 374 2022 131686 10.1016/j.foodchem.2021.131686
Liu F. Sun Z. Wang F. Liu Y. Zhu Y. Du L. Wang D. Xu W. Inhibition of biofilm formation and exopolysaccharide synthesis of Enterococcus faecalis by phenyllactic acid Food Microbiol. 86 2020 103344 10.1016/j.fm.2019.103344
Liu X. Mao B. Gu J. Wu J. Cui S. Wang G. Zhao J. Zhang H. Chen W. Blautia —a new functional genus with potential probiotic properties? Gut Microb. 13 2021 1875796 10.1080/19490976.2021.1875796
Mafart P. Leguérinel I. Modelling the heat stress and the recovery of bacterial spores Int. J. Food Microbiol. 37 1997 131 135 10.1016/S0168-1605(97)00061-5 9310847
Mu W. Yu S. Zhu L. Zhang T. Jiang B. Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound Appl. Microbiol. Biotechnol. 95 2012 1155 1163 10.1007/s00253-012-4269-8 22782253
Mun D. Kyoung H. Kong M. Ryu S. Jang K.B. Baek J. Park K.I. Song M. Kim Y. Effects of Bacillus-based probiotics on growth performance, nutrient digestibility, and intestinal health of weaned pigs J. Anim. Sci. Technol. 63 2021 1314 1327 10.5187/jast.2021.e109 34957446
Murinda S.E. Roberts R.F. Doores S. Evaluation of lactic acid–producing Bacillus and sporolactobacillus for antilisterial activity J. Food Protect. 58 1995 570 572 10.4315/0362-028X-58.5.570
Park J.-H. Kim D.-H. Baik J.-H. Park J.-H. Yoon J.-J. Lee C.-Y. Kim S.-H. Improvement in H2 production from Clostridium butyricum by co-culture with Sporolactobacillus vineae Fuel 285 2021 119051 10.1016/j.fuel.2020.119051
Peters A. Krumbholz P. Jäger E. Heintz-Buschart A. Çakir M.V. Rothemund S. Gaudl A. Ceglarek U. Schöneberg T. Stäubert C. Metabolites of lactic acid bacteria present in fermented foods are highly potent agonists of human hydroxycarboxylic acid receptor 3 PLoS Genet. 15 2019 e1008145 10.1371/journal.pgen.1008145
Rajanikar R.V. Nataraj B.H. Naithani H. Ali S.A. Panjagari N.R. Behare P.V. Phenyllactic acid: a green compound for food biopreservation Food Control 128 2021 108184 10.1016/j.foodcont.2021.108184
Ray C.G. Plorde J.J. Sherris E. Neidhardt F.C. Founders of Sherris Medical Microbiology 2SVV 2014 R ONSˆ SYX 7M1\Ka
RedCorn R. Engelberth A.S. Identifying conditions to optimize lactic acid production from food waste co-digested with primary sludge Biochem. Eng. J. 105 2016 205 213
Rollo A. Sulpizio R. Nardi M. Silvi S. Orpianesi C. Caggiano M. Cresci A. Carnevali O. Live microbial feed supplement in aquaculture for improvement of stress tolerance Fish Physiol. Biochem. 32 2006 167 177 10.1007/s10695-006-0009-2
Sakurai T. Horigome A. Odamaki T. Shimizu T. Xiao J.-Z. Production of hydroxycarboxylic acid receptor 3 (HCA3) ligands by Bifidobacterium Microorganisms 9 2021 10.3390/microorganisms9112397 Article 11
Salminen S. Isolauri E. Salminen E. Clinical uses of probiotics for stabilizing the gut mucosal barrier: successful strains and future challenges Antonie Leeuwenhoek 70 1996 347 358 10.1007/BF00395941 8992950
Sanders M.E. Morelli L. Tompkins T.A. Sporeformers as human probiotics: Bacillus, sporolactobacillus, and brevibacillus Compr. Rev. Food Sci. Food Saf. 2 2003 101 110 10.1111/j.1541-4337.2003.tb00017.x 33451235
Sharma V.K. Sporolactobacilli Wood B.J.B. The Lactic Acid Bacteria vol. 1 1992 Springer US 431 446 10.1007/978-1-4615-3522-5_17
Sharma V.K. Hobson P.N. A sporulation medium for strict anaerobes Lett. Appl. Microbiol. 1 1985 31 32 10.1111/j.1472-765X.1985.tb01482.x
Sharma V.K. Hobson P.N. Properties of a cellulolytic Sporolactobacillus and some non-sporing cellulolytic rods, presumptive clostridia, from an anaerobic digester J. Appl. Bacteriol. 61 1986 257 262 10.1111/j.1365-2672.1986.tb04285.x
Siedler S. Balti R. Neves A.R. Bioprotective mechanisms of lactic acid bacteria against fungal spoilage of food Curr. Opin. Biotechnol. 56 2019 138 146 10.1016/j.copbio.2018.11.015 30504082
Simon O. Micro-organisms as Feed Additives-Probiotics 2005
Soares M.B. Almada C.N. Pereira E.P.R. Ferreira B.M. Balthazar C.F. Khorshidian N. Rocha R.S. Xavier-Santos D. Cruz A.G. Ranadheera C.S. Mortazavian A.M. Gómez-Zavaglia A. Martinez R.C.R. Sant'Ana A.S. Review - sporeforming probiotic bacteria: characteristics, health benefits, and technological aspects for their applications in foods and beverages Trends Food Sci. Technol. 138 2023 453 469 10.1016/j.tifs.2023.06.029
Sorokulova I. Preclinical testing in the development of probiotics: a regulatory perspective with Bacillus strains as an example Clin. Infect. Dis. 46 2008 S92 S95 10.1086/523334 18181731
Swetha T.A. Ananthi V. Bora A. Sengottuvelan N. Ponnuchamy K. Muthusamy G. Arun A. A review on biodegradable polylactic acid (PLA) production from fermentative food waste - its applications and degradation Int. J. Biol. Macromol. 234 2023 123703 10.1016/j.ijbiomac.2023.123703
Swetha T.A. Bora A. Mohanrasu K. Balaji P. Raja R. Ponnuchamy K. Muthusamy G. Arun A. A comprehensive review on polylactic acid (PLA) – synthesis, processing and application in food packaging Int. J. Biol. Macromol. 234 2023 123715 10.1016/j.ijbiomac.2023.123715
Thamacharoensuk T. Kitahara M. Ohkuma M. Thongchul N. Tanasupawat S. Sporolactobacillus shoreae sp. nov. and Sporolactobacillus spathodeae sp. nov., two spore-forming lactic acid bacteria isolated from tree barks in Thailand Int. J. Syst. Evol. Microbiol. 65 2015 1220 1226 10.1099/ijs.0.000084 25634946
Thamacharoensuk T. Tolieng V. Thongchul N. Kodama K. Tanasupawat S. Characterisation of lactic acid producing Sporolactobacillus strains from tree barks in Thailand Ann. Microbiol. 67 2017 215 218 10.1007/s13213-016-1248-9
Thitiprasert S. Jaiaue P. Amornbunchai N. Thammakes J. Piluk J. Srimongkol P. Tanasupawat S. Thongchul N. Association between organic nitrogen substrates and the optical purity of d-lactic acid during the fermentation by Sporolactobacillus terrae SBT-1 Sci. Rep. 14 2024 10522 10.1038/s41598-024-61247-4
Thitiprasert S. Piluk J. Tolieng V. Tanaka N. Shiwa Y. Fujita N. Tanasupawat S. Thongchul N. Draft genome sequencing of Sporolactobacillus terrae SBT-1, an efficient bacterium to ferment concentrated sugar to d-lactic acid Arch. Microbiol. 203 2021 3577 3590 10.1007/s00203-021-02352-0 33961074
Tolieng V. Prasirtsak B. Miyashita M. Shibata C. Tanaka N. Thongchul N. Tanasupawat S. Sporolactobacillus shoreicorticis sp.nov., a lactic acid-producing bacterium isolated from tree bark Int. J. Syst. Evol. Microbiol. 67 2017 2363 2369 10.1099/ijsem.0.001959 28699867
Wang H. Wang L. Ju J. Yu B. Ma Y. Genome sequence of sporolactobacillus laevolacticus DSM442, an efficient polymer-grade d-lactate producer from agricultural waste cottonseed as a nitrogen source Genome Announc. 2013 10.1128/genomea.01100-13
Wardman J.F. Bains R.K. Rahfeld P. Withers S.G. Carbohydrate-active enzymes (CAZymes) in the gut microbiome Nat. Rev. Microbiol. 20 2022 542 556 10.1038/s41579-022-00712-1 35347288
Wee Y.-J. Kim J.-N. Ryu H.-W. Biotechnological production of lactic acid and its recent applications Food Technol. Biotechnol. 44 2006 163 172
Wu B. Yu Q. Zheng S. Pedroso M.M. Guddat L.W. He B. Schenk G. Relative catalytic efficiencies and transcript levels of three d ‐ and two l ‐lactate dehydrogenases for optically pure d ‐lactate production in Sporolactobacillus inulinus Microbiol. Open 8 2019 e00704 10.1002/mbo3.704
Wu B. Yu Q. Zheng S. Pedroso M.M. Guddat L.W. He B. Schenk G. Relative catalytic efficiencies and transcript levels of three d ‐ and two l ‐lactate dehydrogenases for optically pure d ‐lactate production in Sporolactobacillus inulinus MicrobiologyOpen 8 2019 e00704 10.1002/mbo3.704
Yadav M.K. Singh B. Tiwari S.K. Comparative analysis of inhibition-based and indicator-independent colorimetric assay for screening of bacteriocin-producing lactic acid bacteria Probiotics & Antimicro. Prot. 11 2019 687 695 10.1007/s12602-018-9445-4
Yanoshi O.N.A. Spore-bearing lactic acid bacteria isolated from rhizosphere I. Taxonomic studies on Bacillus laevolacticus nov. sp. and Bacillus racemilacticus nov. sp J. Gen. Appl. Microbiol. 13 1967 139 153
Zhang B. Wu L. Liu X. Bao J. Plant proteins as an alternative nitrogen source for chiral purity L-lactic acid fermentation from lignocellulose feedstock Fermentation 8 2022 546 10.3390/fermentation8100546
Zheng L. Liu M. Sun J. Wu B. He B. Sodium ions activated phosphofructokinase leading to enhanced d-lactic acid production by Sporolactobacillus inulinus using sodium hydroxide as a neutralizing agent Appl. Microbiol. Biotechnol. 101 2017 3677 3687 10.1007/s00253-017-8120-0 28190098
Zheng L. Liu M. Sun J. Wu B. He B. Sodium ions activated phosphofructokinase leading to enhanced d-lactic acid production by Sporolactobacillus inulinus using sodium hydroxide as a neutralizing agent Appl. Microbiol. Biotechnol. 101 2017 3677 3687 10.1007/s00253-017-8120-0 28190098
Zheng L. Xu T. Bai Z. He B. Mn2+/Mg2+-dependent pyruvate kinase from a d-lactic acid-producing bacterium Sporolactobacillus inulinus: characterization of a novel Mn2+-mediated allosterically regulated enzyme Appl. Microbiol. Biotechnol. 98 2014 1583 1593 10.1007/s00253-013-4907-9 23695776
Zhou Q. Gu R. Xue B. Li P. Gu Q. Phenyl lactic acid alleviates Samonella Typhimurium-induced colitis via regulating microbiota composition, SCFA production and inflammatory responses Food Funct. 12 2021 5591 5606 10.1039/D1FO00166C 34017972
