Lactobacillus

Lactobacillus is a genus of Gram-positive, aerotolerant anaerobes or microaerophilic, rod-shaped, non-spore-forming bacteria.[2][3] Until 2020, the genus Lactobacillus comprised over 260 phylogenetically, ecologically, and metabolically diverse species; a taxonomic revision of the genus assigned lactobacilli to 25 genera (see § Taxonomy below).[3]

Lactobacillus
Lactobacillus sp. near a squamous epithelial cell
Scientific classification
Domain: Bacteria
Phylum: Bacillota
Class: Bacilli
Order: Lactobacillales
Family: Lactobacillaceae
Genus: Lactobacillus
Beijerinck 1901 (Approved Lists 1980)[1]
Type species
Lactobacillus delbrueckii
(Leichmann 1896) Beijerinck 1901 (Approved Lists 1980)[1]
Species

See text

Lactobacillus species constitute a significant component of the human and animal microbiota at a number of body sites, such as the digestive system, and the female genital system.[4] In women of European ancestry, Lactobacillus species are normally a major part of the vaginal microbiota.[5][6] Lactobacillus forms biofilms in the vaginal and gut microbiota,[7] allowing them to persist during harsh environmental conditions and maintain ample populations.[8] Lactobacillus exhibits a mutualistic relationship with the human body, as it protects the host against potential invasions by pathogens, and in turn, the host provides a source of nutrients.[9] Lactobacilli are among the most common probiotic found in food such as yogurt, and it is diverse in its application to maintain human well-being, as it can help treat diarrhea, vaginal infections, and skin disorders such as eczema.[10]

Metabolism

Lactobacilli are homofermentative, i.e. hexoses are metabolised by glycolysis to lactate as major end product, or heterofermentative, i.e. hexoses are metabolised by the Phosphoketolase pathway to lactate, CO2 and acetate or ethanol as major end products.[11] Most lactobacilli are aerotolerant and some species respire if heme and menaquinone are present in the growth medium.[11] Aerotolerance of lactobacilli is manganese-dependent and has been explored (and explained) in Lactiplantibacillus plantarum (previously Lactobacillus plantarum).[12] Lactobacilli generally do not require iron for growth.[13]

The Lactobacillaceae are the only family of the lactic acid bacteria (LAB) that includes homofermentative and heterofermentative organisms; in the Lactobacillaceae, homofermentative or heterofermentative metabolism is shared by all strains of a genus.[3][11] Lactobacillus species are all homofermentative, do not express pyruvate formate lyase, and most species do not ferment pentoses.[3][11] In L. crispatus, pentose metabolism is strain specific and acquired by lateral gene transfer.[14]

Tryptophan metabolism by human gastrointestinal microbiota ()
Clostridium
sporogenes
Tryptophanase-
expressing
bacteria
IPA
I3A
IPA
I3A
Indoxyl
sulfate
AhR
Intestinal
immune
cells
Intestinal
epithelium
PXR
Mucosal homeostasis:
↓TNF-α
↑Junction protein-
coding mRNAs
L cell
GLP-1
T J
Neuroprotectant:
↓Activation of glial cells and astrocytes
↓4-Hydroxy-2-nonenal levels
↓DNA damage
–Antioxidant
–Inhibits β-amyloid fibril formation
Maintains mucosal reactivity:
↑IL-22 production
Associated with vascular disease:
↑Oxidative stress
↑Smooth muscle cell proliferation
↑Aortic wall thickness and calcification
This diagram shows the biosynthesis of bioactive compounds (indole and certain other derivatives) from tryptophan by bacteria in the gut.[15] Indole is produced from tryptophan by bacteria that express tryptophanase.[15] Clostridium sporogenes metabolizes tryptophan into indole and subsequently 3-indolepropionic acid (IPA),[16] a highly potent neuroprotective antioxidant that scavenges hydroxyl radicals.[15][17][18] IPA binds to the pregnane X receptor (PXR) in intestinal cells, thereby facilitating mucosal homeostasis and barrier function.[15] Following absorption from the intestine and distribution to the brain, IPA confers a neuroprotective effect against cerebral ischemia and Alzheimer's disease.[15] Lactobacillus species metabolize tryptophan into indole-3-aldehyde (I3A) which acts on the aryl hydrocarbon receptor (AhR) in intestinal immune cells, in turn increasing interleukin-22 (IL-22) production.[15] Indole itself triggers the secretion of glucagon-like peptide-1 (GLP-1) in intestinal L cells and acts as a ligand for AhR.[15] Indole can also be metabolized by the liver into indoxyl sulfate, a compound that is toxic in high concentrations and associated with vascular disease and renal dysfunction.[15] AST-120 (activated charcoal), an intestinal sorbent that is taken by mouth, adsorbs indole, in turn decreasing the concentration of indoxyl sulfate in blood plasma.[15]

Genomes

The genomes of lactobacilli are highly variable, ranging in size from 1.2 to 4.9 Mb (megabases).[3] Accordingly, the number of protein-coding genes ranges from 1,267 to about 4,758 genes (in Fructilactobacillus sanfranciscensis and Lentilactobacillus parakefiri, respectively).[19][20] Even within a single species there can be substantial variation. For instance, strains of L. crispatus have genome sizes ranging from 1.83 to 2.7 Mb, or 1,839 to 2,688 open reading frames.[21] Lactobacillus contains a wealth of compound microsatellites in the coding region of the genome, which are imperfect and have variant motifs.[22] Many lactobacilli also contain multiple plasmids. A recent study has revealed that plasmids encode the genes which are required for adaptation of lactobacilli to the given environment.[23]

Species

The genus Lactobacillus comprises the following species:[24][25]

  • Lactobacillus acetotolerans Entani et al. 1986
  • Lactobacillus acidophilus (Moro 1900) Hansen and Mocquot 1970 (Approved Lists 1980)
  • "Lactobacillus alvi" Kim et al. 2011
  • Lactobacillus amylolyticus Bohak et al. 1999
  • Lactobacillus amylovorus Nakamura 1981
  • Lactobacillus apis Killer et al. 2014
  • "Lactobacillus backi" Bohak et al. 2006
  • Lactobacillus bombicola Praet et al. 2015
  • Lactobacillus colini Zhang et al. 2017
  • Lactobacillus crispatus (Brygoo and Aladame 1953) Moore and Holdeman 1970 (Approved Lists 1980)
  • Lactobacillus delbrueckii (Leichmann 1896) Beijerinck 1901 (Approved Lists 1980)
  • Lactobacillus equicursoris Morita et al. 2010
  • Lactobacillus fornicalis Dicks et al. 2000
  • Lactobacillus gallinarum Fujisawa et al. 1992
  • Lactobacillus gasseri Lauer and Kandler 1980
  • Lactobacillus gigeriorum Cousin et al. 2012
  • "Lactobacillus ginsenosidimutans" Jung et al. 2013
  • Lactobacillus hamsteri Mitsuoka and Fujisawa 1988
  • Lactobacillus helsingborgensis Olofsson et al. 2014
  • Lactobacillus helveticus (Orla-Jensen 1919) Bergey et al. 1925 (Approved Lists 1980)
  • Lactobacillus hominis Cousin et al. 2013
  • Lactobacillus iners Falsen et al. 1999
  • Lactobacillus intestinalis (ex Hemme 1974) Fujisawa et al. 1990
  • Lactobacillus jensenii Gasser et al. 1970 (Approved Lists 1980)
  • "Lactobacillus jinshani" Yu et al. 2020
  • Lactobacillus johnsonii Fujisawa et al. 1992
  • Lactobacillus kalixensis Roos et al. 2005
  • Lactobacillus kefiranofaciens Fujisawa et al. 1988
  • Lactobacillus kimbladii Olofsson et al. 2014
  • Lactobacillus kitasatonis Mukai et al. 2003
  • Lactobacillus kullabergensis Olofsson et al. 2014
  • Lactobacillus melliventris Olofsson et al. 2014
  • Lactobacillus mulieris Rocha et al. 2020
  • Lactobacillus nasalidis Suzuki-Hashido et al. 2021
  • Lactobacillus panisapium Wang et al. 2018
  • Lactobacillus paragasseri Tanizawa et al. 2018
  • Lactobacillus pasteurii Cousin et al. 2013
  • Lactobacillus porci Kim et al. 2018
  • Lactobacillus psittaci Lawson et al. 2001
  • "Lactobacillus raoultii" Nicaise et al. 2018
  • Lactobacillus rodentium Killer et al. 2014
  • Lactobacillus rogosae Holdeman and Moore 1974 (Approved Lists 1980)
  • Lactobacillus taiwanensis Wang et al. 2009
  • "Lactobacillus thermophilus" Ayers and Johnson 1924
  • "Lactobacillus timonensis" Afouda et al. 2017
  • Lactobacillus ultunensis Roos et al. 2005
  • Lactobacillus xujianguonis Meng et al. 2020

Taxonomy

The genus Lactobacillus currently contains 44 species which are adapted to vertebrate hosts or to insects.[3] In recent years, other members of the genus Lactobacillus (formerly known as the Leuconostoc branch of Lactobacillus) have been reclassified into the genera Atopobium, Carnobacterium, Weissella, Oenococcus, and Leuconostoc. The Pediococcus species P. dextrinicus has been reclassified as a Lapidilactobacillus dextrinicus [3][26] and most lactobacilli were assigned to Paralactobacillus or one of the 23 novel genera of the Lactobacillaceae.[3] Two websites inform on the assignment of species to the novel genera or species (http://www.lactobacillus.uantwerpen.be/; http://www.lactobacillus.ualberta.ca/).

The 23 new genera of 2020
Genus Meaning of the genus name Properties of the genus
Lactobacillus Rod-shaped bacillus from milk Type species: L. delbrueckii.

Homofermentative with strain-specific ability to ferment pentoses, thermophilic, vancomycin-sensitive, adapted to vertebrate or insect hosts.

Holzapfelia Wilhelm Holzapfel’s lactobacilli Type species: H. floricola.

Homofermentative, vancomycin sensitive, unknown ecology but likely host-adapted.

Amylolactobacillus Starch degrading lactobacilli Type species: A. amylophilus.

Homofermentative, vancomycin sensitive, extracellular amylases are frequent, unknown ecology but likely host-adapted.

Bombilactobacillus Lactobacilli from bees and bumblebees Type species: B. mellifer.

Homofermentative, thermophilic, vancomycin resistant, small genome size, adapted to bees and bumblebees

Companilactobacillus Companion-lactobacillus, growing in association with other lactobacilli in cereal, meat and vegetable fermentations Type species: C. alimentarius.

Homofermentative with strain- or species specific ability to ferment pentoses, vancomycin resistant, unknown ecology, likely nomadic

Lapidilactobacillus Lactobacilli from stones Type species: L. concavus.

Homofermentative with strain- or species specific ability to ferment pentoses, vancomycin resistant, unknown ecology.

Agrilactobacillus Lactobacilli from fields Type species: A. composti.

Homofermentative, aerotolerant and vancomycin resistant. Genome size, G+C content of the genome and the source of the two species suggest a free-living lifestyle of the genus.

Schleiferilactobacillus Karl Heinz Schleifer’s lactobacilli Type species: S. perolens.

Homofermentative, vancomycin resistant, aerotolerant. Schleiferilactobacillus spp. have a large genome size, ferment a wide range of carbohydrates, and spoil beer and dairy products by copious production of diacetyl.

Loigolactobacillus (Food) spoiling lactobacilli Type species: L. coryniformis.

Homofermentative, vancomycin resistant, mesophilic or psychrotrophic organisms.

Lacticaseibacillus Lactobacilli related to cheese Type species: L. casei.

Homofermentative, vancomycin resistant; many species ferment pentoses, and are resistant to oxidative stress. L. casei and related species have a nomadic lifestyle.

Latilactobacillus Wide-spread lactobacilli Type species: L. sakei.

Homofermentative, mesophilic free living and environmental lactobacilli. Many strains are psychrotrophic and grow below 8 °C.

Dellaglioa Franco Dellaglio’s lactobacilli Type species: D. algidus.

Homofermentative, vancomycin resistant, aerotolerant and psychrophilic.

Liquorilactobacillus Lactobacilli from liquor or liquids Type species: L. mali.

Homofermentative, vancomycin resistant, motile organisms growing in liquid, plant-associated habitats. Many liquorilactobacilli produce EPS from sucrose and degrade fructans with extracellular fructanases.

Ligilactobacillus Uniting (host adapted) lactobacilli Type species: L. salivarius.

Homofermentative, vancomycin resistant, most ligilactobacilli are host adapted and many strains are motile. Several strains of Ligilactobacillus express urease to withstand gastric acidity.

Lactiplantibacillus Lactobacilli related to plants Type species: L. plantarum.

Homofermentative, vancomycin resistant organisms with a nomadic lifestyle that ferment a wide range of carbohydrates; most species metabolise phenolic acids by esterase, decarboxylase and reductase activities. L. plantarum expresses pseudocatalase and nitrate reductase activities.

Furfurilactobacillus Lactobacilli from bran Type species: F. rossiae.

Heterofermentative, vancomycin resistant, with large genome size, broad metabolic potential and unknown ecology.

Paucilactobacillus Lactobacilli fermenting few carbohydrates Type species: P. vaccinostercus.

Heterofermentative, vancomycin resistant, mesophilic or psychrotrophic, aerotolerant, most strains ferment pentoses but not disaccharides.

Limosilactobacillus Slimy (biofilm-forming) lactobacilli Type species: L. fermentum.

Heterofermentative, thermophilic, vancomycin resistant with two exceptions, Limosilactobacillus species are vertebrate host adapted and generally form exopolysaccharides from sucrose to support biofilm formation in the upper intestine of animals.

Fructilactobacillus Fructose-loving lactobacilli Type species: F. fructivorans.

Heterofermentative, vancomycin resistant, mesophilic, aerotolerant, small genome size. Fructilactobacilli are adapted to narrow ecological niches that relate to insects, flowers, or both.

Acetilactobacillus Lactobacilli from vinegar Type species: A. jinshani.

Heterofermentative, vancomycin resistant, grow in the pH range of 3 – 5; fermenting disaccharides and sugar alcohols but few hexoses and no pentoses.

Apilactobacillus Lactobacilli from bees Type species: A. kunkeei.

Heterofermentative, vancomycin resistant, small genome size, fermenting only few carbohydrates, adapted to bees and / or flowers.

Levilactobacillus (Dough)-leavening lactobacilli Type species: L. brevis.

Heterofermentative, vancomycin resistant, mesophilic or psychrotrophic, metabolise agmatine, environmental or plant-associated lifestyle.

Secundilactobacillus Second lactobacilli, growing after other organisms depleted hexoses Type species: S. collinoides.

Heterofermentative, vancomycin resistant, mesophilic or psychrotrophic, environmental or plant-associated lifestyle. Adapted to hexose-depleted habitats, most strains do not reduce fructose to mannitol but metabolize agmatine and diols.

Lentilactobacillus Slow (growing) lactobacilli Type species: L. buchneri.

Heterofermentative, vancomycin resistant, mesophilic, fermenting a broad spectrum of carbohydrates. Most lentilactobacilli are environmental or plant-associated, metabolise agmatine and convert lactate and / or diols. L. senioris and L. kribbianus form an outgroup to the genus; both species were isolated from vertrebrates and may transition to a host-adapted lifestyle.

Phylogeny

The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature[24] and the phylogeny is based on whole-genome sequences.[3]

 
Lactobacillus
 
 
 
 
 
 
 
 
 
 
 
 

Lactobacillus gallinarum

 
 

Lactobacillus helveticus

 
 
 

Lactobacillus acidophilus

 
 
 

Lactobacillus ultunensis

 
 
 

Lactobacillus crispatus

 
 
 
 

Lactobacillus amylovorus

 
 

Lactobacillus kitasatonis

 
 
 
 

Lactobacillus kefiranofaciens

 
 
 

Lactobacillus hamsteri

 
 
 
 
 

Lactobacillus gigeriorum

 
 

Lactobacillus pasteurii

 
 
 
 

Lactobacillus kilaxensis

 
 
 

Lactobacillus intestinalis

 
 
 

Lactobacillus amylolyticus

 
 

Lactobacillus xujianguonis

 
 
 
 
 
 
 
 

Lactobacillus acetotolerans

 
 
 
 
 

Lactobacillus apis

 
 

Lactobacillus panisapium

 
 
 

Lactobacillus bombicola

 
 
 
 
 

Lactobacillus helsingborgensis

 
 

Lactobacillus melliventris

 
 
 
 

Lactobacillus kimbladii

 
 

Lactobacillus kullabergensis

 
 
 
 
 
 
 
 

Lactobacillus porci

 
 
 

Lactobacillus delbrueckii

 
 

Lactobacillus equicursoris

 
 
 
 
 
 

Lactobacillus psittaci

 
 
 

Lactobacillus fornicalis

 
 

Lactobacillus jensenii

 
 
 
 
 
 

Lactobacillus rodentium

 
 
 

Lactobacillus iners

 
 
 

Lactobacillus colini

 
 
 

Lactobacillus hominis

 
 
 

Lactobacillus johnsonii

 
 
 

Lactobacillus taiwanensis

 
 
 

Lactobacillus gasseri

 
 

Lactobacillus paragasseri

 
 
 
 
 
 
 
 
 
outgroup

Holzapfelia

 
 

Human health

Vaginal tract

The female genital tract is one of the principal colonisation sites for human microbiotic, and there is interest in the relationship between their presence and human health, with a domination by a single species being correlated with general welfare and good outcomes in pregnancy. In around 70% of women, a Lactobacillus species is dominant, although that has been found to vary between American women of European origin and those of African origin, the latter group tending to have more diverse vaginal microbiota. Similar differences have also been identified in comparisons between Belgian and Tanzanian women.[5]

Interactions with pathogens

Lactobacilli produce hydrogen peroxide which inhibits the growth and virulence of the fungal pathogen Candida albicans in vitro and in vivo.[27][28] In vitro studies have also shown that lactobacilli reduce the pathogenicity of C. albicans through the production of organic acids and certain metabolites.[29] Both the presence of metabolites, such as sodium butyrate, and the decrease in environmental pH caused by the organic acids reduce the growth of hyphae in C. albicans, which reduces its pathogenicity.[29] Lactobacilli also reduce the pathogenicity of C. albicans by reducing C. albicans biofilm formation.[29] Biofilm formation is reduced by both the competition from lactobacilli, and the formation of defective biofilms which is linked to the reduced hypha growth mentioned earlier.[29] On the other hand, following antibiotic therapy, certain Candida species can suppress the regrowth of lactobacilli at body sites where they cohabitate, such as in the gastrointestinal tract.[27][28]

In addition to its effects on C. albicans, Lactobacillus sp. also interact with other pathogens. For example, Limosilactobacillus reuteri (formerly Lactobacillus reuteri) can inhibit the growth of many different bacterial species by using glycerol to produce the antimicrobial substance called reuterin.[30] Another example is Ligilactobacillus salivarius (formerly Lactobacillus salivarius), which interacts with many pathogens through the production of salivaricin B, a bacteriocin.[31]

Probiotics

Fermentive bacteria like lactic acid bacteria (LAB) produce hydrogen peroxide which protects themselves from oxygen toxicity. The accumulation of hydrogen peroxide in growth media, and its antagonistic effects on Staphylococcus aureus and Pseudomonas, have been demonstrated by researchers. LAB cultures have been used as starter cultures to create fermented foods since the beginning of the 20th century. Elie Metchnikoff won a Nobel prize in 1908 for his work on LAB.[32]

Lactobacilli administered in combination with other probiotics benefits cases of irritable bowel syndrome (IBS), although the extent of efficacy is still uncertain.[33] The probiotics help treat IBS by returning homeostasis when the gut microbiota experiences unusually high levels of opportunistic bacteria.[9] In addition, lactobacilli can be administered as probiotics during cases of infection by the ulcer-causing bacterium Helicobacter pylori.[34] Helicobacter pylori is linked to cancer, and antibiotic resistance impedes the success of current antibiotic-based eradication treatments.[34] When probiotic lactobacilli are administered along with the treatment as an adjuvant, its efficacy is substantially increased and side effects may be lessened.[34]

Vaginal squamous cell with normal vaginal flora versus bacterial vaginosis on Pap stain. Normal vaginal flora (left) is predominantly rod-shaped Lactobacilli, whereas in bacterial vaginosis (right) there is an overgrowth of bacteria, which can be of various species.

Also, lactobacilli are used to help control urogenital and vaginal infections, such as bacterial vaginosis (BV). Lactobacilli produce bacteriocins to suppress pathogenic growth of certain bacteria,[35] as well as lactic acid and H2O2 (hydrogen peroxide). Lactic acid lowers the vaginal pH to around 4.5 or less, hampering the survival of other bacteria, and H2O2 reestablishes the normal bacterial microbiota and normal vaginal pH.[35] In children, lactobacilli such as Lacticaseibacillus rhamnosus (previously L. rhamnosus) are associated with a reduction of atopic eczema, also known as dermatitis, due to anti-inflammatory cytokines secreted by this probiotic bacteria.[9] In addition, lactobacilli with other probiotic[36] organisms in ripened milk and yogurt aid development of immunity in the mucous intestine in humans by raising the number of LgA (+).

Oral health
Dental caries

Some lactobacilli have been associated with cases of dental caries (cavities). Lactic acid can corrode teeth, and the Lactobacillus count in saliva has been used as a "caries test" for many years. Lactobacilli characteristically cause existing carious lesions to progress, especially those in coronal caries. The issue is, however, complex, as recent studies show probiotics can allow beneficial lactobacilli to populate sites on teeth, preventing streptococcal pathogens from taking hold and inducing dental decay. The scientific research of lactobacilli in relation to oral health is a new field and only a few studies and results have been published.[37][38] Some studies have provided evidence of certain Lactobacilli which can be a probiotic for oral health.[39] Some species, but not all, show evidence in defense to dental caries.[39] Due to these studies, there have been applications of incorporating such probiotics in chewing gum and lozenges.[39] There is also evidence of certain Lactobacilli that are beneficial in the defense of periodontal disease such as gingivitis and periodontitis.[39]

Food production

Lactobacilli comprise most food fermenting lactic acid bacteria [40][41] and are used as starter cultures in industry for controlled fermentation in the production of wine, yogurt, cheese, sauerkraut, pickles, beer, cider, kimchi, cocoa, kefir, and other fermented foods, as well as animal feeds and the bokashi soil amendment. Lactobacillus species are dominant in yogurt, cheese, and sourdough fermentations.[40][41] The antibacterial and antifungal activity of lactobacilli relies on production of bacteriocins and low molecular weight compounds that inhibits these microorganisms.[42][43]

Sourdough bread is made either spontaneously, by taking advantage of the bacteria naturally present in flour, or by using a "starter culture", which is a symbiotic culture of yeast and lactic acid bacteria growing in a water and flour medium.[44] The bacteria metabolize sugars into lactic acid, which lowers the pH of their environment and creates the signature sourness associated with yogurt, sauerkraut, etc.

In many traditional pickling processes, vegetables are submerged in brine, and salt-tolerant lactobacilli feed on natural sugars found in the vegetables. The resulting mix of salt and lactic acid is a hostile environment for other microbes, such as fungi, and the vegetables are thus preserved—remaining edible for long periods.

Lactobacilli, especially pediococci and L. brevis, are some of the most common beer spoilage organisms. They are, however, essential to the production of sour beers such as Belgian lambics and American wild ales, giving the beer a distinct tart flavor.

See also
  • Lactobacillus L. anticaries
  • Lactic acid fermentation
  • MRS agar
  • Pediococcus
  • Probiotics
  • Proteobiotics
  • Carbon monoxide-releasing molecules

References
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  10. Inglin R (2017). Combined Phenotypic-Genotypic Analyses of the Genus Lactobacillus and Selection of Cultures for Biopreservation of Fermented Food. ETHZ research collection (Ph.D. thesis). ETH Zurich. doi:10.3929/ethz-b-000214904. hdl:20.500.11850/214904.
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  14. Li, Qing; Gänzle, Michael G. (December 2020). "Characterization of two extracellular arabinanases in Lactobacillus crispatus". Applied Microbiology and Biotechnology. 104 (23): 10091–10103. doi:10.1007/s00253-020-10979-0. ISSN 1432-0614. PMID 33119797. S2CID 226203002.
  15. Zhang LS, Davies SS (April 2016). "Microbial metabolism of dietary components to bioactive metabolites: opportunities for new therapeutic interventions". Genome Med. 8 (1): 46. doi:10.1186/s13073-016-0296-x. PMC 4840492. PMID 27102537. Lactobacillus spp. convert tryptophan to indole-3-aldehyde (I3A) through unidentified enzymes [125]. Clostridium sporogenes convert tryptophan to IPA [6], likely via a tryptophan deaminase. ... IPA also potently scavenges hydroxyl radicals
    Table 2: Microbial metabolites: their synthesis, mechanisms of action, and effects on health and disease
    Figure 1: Molecular mechanisms of action of indole and its metabolites on host physiology and disease
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