Sneathia amnii

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Introduction

Have you ever wondered exactly what microbes are in your normal microbiota? The microorganisms within our normal microbiota live within us and remain with us every day! Bacteria of the genus Sneathia were isolated from blood cultures taken from obstetric patients with post-partum fever, two newborn children and a 100-year-old woman in 1995. The bacteria are Gram stain negative, anaerobic, rod-shaped bacteria are emerging as potential pathogens of the female reproductive tract (Eisenberg et al, 2018). The species Sneathia, which had been a part of the genus Leptotrichia prior to its reclassification, is a part of the normal microbiota of the genitourinary tracts of men and women. Sneathia have a significant role in obstetrics and the health of women’s reproductive systems. This bacteria is of particular concern for women because it most commonly inhabits the human vagina and poses risk, especially for those who are pregnant. Sneathia has been known to cause preterm delivery and is heavily present in the blood of newborn babies, but it doesn’t just stop there. They are also associated with numerous clinical conditions such as bacterial vaginosis, preeclampsia, miscarriages, post-partum bacteremia and some other invasive infections (Harwich et al, 2020). Sneathia species also exhibit a significant correlation with sexually transmitted diseases and cervical cancer. The limited forms of carbohydrates that S. amnii is able to metabolize include glucose, maltose, glycogen and glucosamine (Harwich et al, 2020). Due to the very fixed nutrient requirement of Sneathia, it is difficult to cultivate in the lab. A consequence of this is that very is little known about its biology or its pathogenic capabilities. They are not able to ferment starch, mucin and mannose. In order to learn more about how pathogenic Sneathia are in terms of pelvic inflammatory disease, more studies will need to be done. Pelvic inflammatory disease is an infection of particular concern for women because it effects the reproductive organs and can possibly lead to infertility or chronic pelvic pain.


Electron Micrographs of S. amnii. S. amnii were fixed to either glass cover slips or copper grids, and visualized by SEM (a) or TEM (b), respectively by Harwich Jr et al. (2012) https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3535699/


Gram stain of Sneathia amnii by Duployez et al. (2020). Gram stain from colonies on blood agar, image taken at magnification 1000x. Presence of long and short Gram-negative rods. https://reader.elsevier.com/reader/sd/pii/S1075996420301335?token=E22DB79E5100C93C86CD14DBA659C6A7B8C73FD251F2702FCB1FD5A4ADBB24B26E5A134903DB9E32EFA6815BE5CE4DEB

Classification

Higher order taxa

Bacteria; Fusobacteria; Fusobacteriia; Fusobacteriales; Leptotrichiaceae

Species Sneathia amnii, Sneathia sanguinegens NCBI: https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=168808 JGI: https://gold.jgi.doe.gov/project?id=Gp0121048 Genus species

Phylogenetic Relatedness

Phylogenetic Relatedness Researchers set out to isolate a clone from the mid-vaginal sample that was taken from the young African American woman with a goal of better defining the role of novel S. amnii. She was presenting with symptoms of preterm labor after carrying her child for only 26 weeks. The 16S rRNA gene of the clone was completely sequenced and then compared to the 16S rDNAs from various members of the Fusobacteriaceae family. This enabled researchers to assess the phylogenetic relationships between the different bacteria. The alignment showed that the 16S rDNA of the Sneathia amnii isolate is almost 99.8% identical to the 16S rDNA of the Leptotrichia amnii isolate. The 16S rDNA of the Sneathia isolate showed 94.7% overall sameness to S. sanguinegens, but only 84.4% overall sameness to Leptotrichia buccalis, the type species of the genus Leptotrichia.

Presented is the maximum likelihood phylogenetic tree of S. amnii and its related organisms within the family Fusobacteriaceae (Harwich Jr et al., 2012) https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3535699/

Ecological Habitat

 Sneathia are most commonly found in the genitourinary tract but are also found as pathogens in the amniotic fluid of pregnant women (Harwich et al., 2012). It plays a large role in vaginal and reproductive health, as it is found in the microbiome of both the male and female urogenital tracts. In women, Sneathia can contribute to serious complications of birth, such as preterm labor or miscarriage, bacterial vaginosis, inflammation, histological amnionitis and amnionitis. It’s very important to remember that Sneathia is not only found in women! In males, the microbe contributed to and was associated with sexually transmitted diseases.

Figure 1: This heat map shows the vaginal microbiota community state types.8 Compared to the other microbes that are present in community state 5, Sneathia are of the most prevalent species, which is denoted by the darker blue color. The bacteria in community state type 5 are the ones that are most microbially similar to bacterial vaginosis. Sneathia are associated with the clinical condition of bacterial vaginosis. Credit: Swidsinski et al., 2017

Figure 2: This picture shows the vaginal epithelium under 1000x magnification from a post-menopausal, which was taken with unstructured biofilm.7 This is where Sneathia is most likely to interact in the vagina and receive their nutrients but are found can be found as a pathogen in the amniotic fluid. Credit: Smith and Ravel, 2017


 Human clinical specimen are the main sources of isolation. The genus is most commonly found in clinical samples from the mid-vaginal wall area or amniotic fluid. In order to identify Sneathia amnii from a sample, the V1-V3 region of the 16s-ribosomal-RNA-endocded gene is amplified (Harwich et al., 2012). The analysis was able to clearly differentiate S. amnii from S. sanguinegens. It turns out that these two species are approximately only 91% to 93% identical to one another; this actually makes them distant. The specific growth requirements of S. amnii makes it a difficult species to culture in the lab with common microbiological techniques.

 Sneathia amnii’s enviornment is one that is very acidic. The normal pH of the vagina is about 4 but ranges from 3.5 to 4.5. The normal pH of amniotic fluid is 6.5 or higher. When Sneathia amnii is present, pH levels will rise and become even more basic (Ray et al., 2017). The temperature is about the same as body temperature, a range of 36 to 37 degrees Celsius. The human body does contain oxygen but S. amnii is an aerotolerant anaerobe that protects itself from reactive oxygen molecules and avoid their use. The area receives little to no amounts of light and is moist. There is lactic acid, urea, estrogen, progesterone, luteinizing hormone and amines, including isobutylamine, phenethylamine, putrescine, cadaverine, and tyramine, found in vaginal secretions (Wolrath et al., 2001).

Significance to the Environment

 S. amnii has very complicated growth requirements. It is able to metabolize few carbohydrates, including glucose, maltose, glycogen and glucosamine. This species, however, lacks the ability to ferment starch, mucin, fructose, sucrose or mannose (Eisenberg et al., 2018). S. amnii’s fermentative style of metabolism leaves lactic acid, formic acid, a small amount of acetic acid and sometimes succinic acids as the waste products after metabolizing glucose. Since the epithelium of the vagina produces a lot of glucose, especially when a woman is at reproductive age, S. amnii is able to use this carbohydrate source despite its reduced metabolic capabilities with other carbohydrates.

 More information about fermentative metabolism of glucose: o https://umaine.edu/carbohydrates/carbohydrate-digestion/fermentation/ (University of Maine, n.d.)

 Sneathia strains tend to be susceptible to and best treated with antimicrobials, such as metronidazole, but can be resistant to erythromycin, kanamycin, vancomycin, aminoglycosides, and fluoroquinolone. We know that S. amnii is one of the anaerobic microbes that plays a role in the development of bacterial vaginosis. The overuse of metronidazole in treatment may have caused the recent relative resistance to it (Eschenbach, 2007). This conclusion comes from a study that showed increase failure rate of a treatment course using metronidazole spanning over two weeks of time.

Ecological Lifestyle and Interactions

 Sneathia amnii is an opportunistic microbe that is emerging as being increasingly pathogenic. It most commonly associates itself with humans, as it is mostly found in the female urogenital tracts. Its presence causes infections, and it has also been found in cultured blood samples and fluid of the joints (Eisenberg et al., 2018). When Sneathia amnii’s genome was sequenced, there were potential cytotoxins revealed that had the ability to kill eukaryotic cells in the test tube or culture dish (Fettweis et al., 2019). Microbes that were phenotypically similar to Sneathia were found in the urine of cows and female sheep; the effect of the microbe on uterine health in these animals is yet to be clearly defined (Eisenberg et al., 2018).

Lewis et al (2017) published a figure in their study showing the sociological framework for the determinants of one’s “normal” vaginal microbiome. All these factors have potential for determining what microbes Sneathia amnii will be interacting with in the vagina. For example, women of European and African descent can have differing profiles for their vaginal microbiome (Fettweis et al., 2019). A woman of African descent is more likely to have an abundance of L. crispatus. Figure Link: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743080/#:~:text=Significant%20evidence%20now%20indicates%20that,is%20optimal%20for%20vaginal%20health.&text=Recent%20studies%20have%20shown%20that,the%20absence%20of%20bacterial%20vaginosis

 Sneathia amnii can be associated with other microbes that makeup the normal vaginal microbiome, along with those that contribute to bacterial vaginosis. One of the microbes it’s associated with is the uncultured Bacterial Vaginosis Associated Bacterium (BVAB1), also known as Candidatus Lachnocurva vaginae. This microbe is held responsible for interminable bacterial vaginosis (BV), inflammation of the vagina and harmful childbirths (Holm et al., 2020). Lactobacilli make up most of the microbe population in the vagina of women who are at reproductive age. Lactobacillus crispatus (https://microbewiki.kenyon.edu/index.php/Lactobacillus_crispatus), Lactobacillus iners, Lactobacillus gasseri, and Lactobacillus jensenii are the main species of Lactobacillus in the vagina. S. amnii interact with these species as it fights to carry on its pathogenic processes. Lactobacilli’s ability to inhibit pro-inflammatory cytokines from initiating their performance comes as a threat to Sneathia. Lactobacilli can also keep bacteria from forming attachments to the vaginal epithelium and produce lactic acid to kill other bacteria (Witkin and Linares, 2017). Since BV is associated with a significant reduction of the lactobacilli morphotypes, S. amnii also gets to interact with bacteria that are anaerobic and short rodded and coccoid (Harwich et al., 2012). The anerobic bacteria include Gardnerella vaginalis (https://microbewiki.kenyon.edu/index.php/Gardenerella_vaginalis), Prevotella spp (https://microbewiki.kenyon.edu/index.php/Prevotella), Peptostreptococcus (https://microbewiki.kenyon.edu/index.php/Peptostreptococcus_anaerobius), Bacteroides spp, Mobiluncus spp., Ureaplasma urelyticum (https://microbewiki.kenyon.edu/index.php/Ureaplasma_urealyticum) and Mycoplasma hominis (https://microbewiki.kenyon.edu/index.php/Mycoplasma_hominis).

 The biological interaction between Lactobacilli and Sneathia are very important in the vaginal environment. Bacteria of the Lactobacillus species are able to prevent other bacteria from binding to the vagina’s epithelium, in part with their lactic acid production. It sets out to stop any and all functions of pro-inflammatory cytokines. Secretion of lactic acid allows for Lactobacilli to kill other bacteria or at least put a stop to their growth (Witkin and Linares, 2017). Lactic acid is sometime released with bacteriocins to ensure efficacy. Bacteriocins are just additional antimicrobial factors. Lactic acid can further stimulate transcription of genes and DNA restoration by restricting histone deacetylases. Autophagy is induced when lactic acid is released, causing the harmful cells to degrade themselves and maintain normal functioning and processes. Lactobacilli’s proficiency in preventing infections without having to initiate any inflammation promotes fertility and successful pregnancies in women (Witkin and Linares, 2017).

Significance to Humans

 S. amnii has very complicated growth requirements. It is able to metabolize few carbohydrates, including glucose, maltose, glycogen and glucosamine. This species, however, lacks the ability to ferment starch, mucin, fructose, sucrose or mannose (Eisenberg et al., 2018). S. amnii’s fermentative style of metabolism leaves lactic acid, formic acid, a small amount of acetic acid and sometimes succinic acids as the waste products after metabolizing glucose. Since the epithelium of the vagina produces a lot of glucose, especially when a woman is at reproductive age, S. amnii is able to use this carbohydrate source despite its reduced metabolic capabilities with other carbohydrates.

 More information about fermentative metabolism of glucose: o https://umaine.edu/carbohydrates/carbohydrate-digestion/fermentation/ (University of Maine, n.d.)

 Sneathia strains tend to be susceptible to and best treated with antimicrobials, such as metronidazole, but can be resistant to erythromycin, kanamycin, vancomycin, aminoglycosides, and fluoroquinolone. We know that S. amnii is one of the anaerobic microbes that plays a role in the development of bacterial vaginosis. The overuse of metronidazole in treatment may have caused the recent relative resistance to it (Eschenbach, 2007). This conclusion comes from a study that showed increase failure rate of a treatment course using metronidazole spanning over two weeks of time.

Cell Structure

 Individual cells of S. amnii lack flagellar proteins and pilin when observed under a microscope. S. amnii doesn’t have genes that code for those proteins nor were they indicated with varying forms of electron microscopy. Sneathia amnii’s cells can have different shapes. There can be a mixture of rods longer than 10 micrometers that can be chains of short rods attached end to end, shorter rods and cocci (Eisenberg et al., 2018). Older cultures of Sneathia amnii are shown to be more likely to have the short rods, which are representative of variants of S. amnii that don’t have a cell wall (Eisenberg et al., 2018). Its cells are also fusiform or shaped in a spindle (Holm et al., 2020).

 Colonies of S. amnii can show pleomorphism, meaning that the cells can change their form and function. The change in structure and function is triggered by varying conditions of the environment such as changes in pH or presence of an antibiotic. Sneathia amnii is Gram-stain-negative, so for this form of test for cell differentiation it does not keep the violet color from the stain. Instead of purple, it is red (Harwich et al., 2012). This would mean that the cell would be made up of a single thin layer of peptidoglycan. The peptidoglycan provides strength to the cell wall, especially when antibiotics are attacking, and it is involved in cell reproduction. Sneathia amnii grows best when no oxygen is present. Although anaerobic conditions are most ideal, there can still be a small amount of growth in aerobic conditions. Optimal temperature would be similar to that of the body, which would be close to 37° Celsius (Harwich et al., 2012). Conditions where there is no UV present and a low, or acidic, pH are ideal. On a chocolate agar the colonies were gray in color, flat, crystalline and its diameter was approximately 1 millimeter (Eisenberg et al., 2018). When observed on a Brain Heart Infusion agar that had fresh human blood, colonies of S. amnii had a diameter or about 2 millimeters and were mucoid, raised and amorphous (Eisenberg et al., 2018).

 S. amnii is non-motile meaning that it lacks the ability to move and remains in place (Eisenberg et al., 2018). This may explain the lack of flagellar proteins. The antibiotic resistance profile of S. amnii showed that it is highly resistant to nafcillin, which is not uncommon for bacteria that are Gram negative. Nafcillin has little to no effect on Gram-negative bacteria because of the outer membrane that is very impermeable. S. amnii is more sensitive to metronidazole, a common antibiotic for bacterial vaginosis, than other Gram-negative bacteria (Eisenberg et al., 2018). Gram-negative bacteria, like S. amnii, are assumed to be resistant to vancomycin for the most part. Vancomycin is too big to be able to easily bypass the membrane. Interestingly enough, Sneathia amnii shows sensitivity to vancomycin despite being Gram negative which may go to show that its membrane may have a different makeup than other Gram-negative microbes (Eisenberg et al., 2018). Since most Gram-negative bacteria are resistant to vancomycin, sensitivity to vancomycin could be used as a secondary test to actually using the Gram stain. S. amnii is highly resistant to tetracycline and ciprofloxacin, in dosages over 50 and 25 micrograms per milliliters, respectively (Eisenberg et al., 2018).

Cell Metabolism

 It has the ability to grow on chocolate agar and doesn’t need blood on the agar to grow unlike other bacteria in the genus. Its Gram-negative outer membrane is compositionally different than other Gram-negative microbes; this can be attributed to the amount permeases and transporters that are present (Eisenberg et al., 2018). Sneathia amnii’s genome shows the code for two MATE efflux family homologs, ensuring its resistance to antibiotics. S. amnii’s gram negative membrane allows it to be resistant to antibiotics and carry on its pathogenic processes. The MATE efflux family homologs serve this same purpose; any microbe with this in its genome can be single or multi-drug resistant to antimicrobial medicines and promote increased survival. A microbe being Gram-negative is already beneficial in and of itself when interacting with the environment because of the “protective capsule” formed to “hide” from the antibiotics (Eisenberg et al., 2018).

 This bacteria has the capabilities to use glycogen for energy but it cannot use many other carbon sources for growth (Harwich et al., 2012). It feeds off of the glycogen that is produced by the cells of vaginal epithelial of women. Women’s cells start to produce these sugars once they are of reproductive age. Cultures have shown that when human serum is present, S. amnii is able to grow more. Human serum has the ability to carry nutrients into the cell and aid in cell growth. Its genome showed that phosphotransferase systems were present in S. amnii. Phosphotransferase systems are a system involving enzymes for bacteria to take in the sugars, such as mannose, galactitol and cellobiose, and use them for energy (Deutscher et al., 2008). It is unusual that S. amnii even has this mechanism to help with metabolism because it is known that this bacteria is unable to metabolize mannose or glucose (Eisenberg et al., 2018).

Genome Structure, Content, and/or Gene Expression

Genome Project: https://www.genome.gov/25520338/online-education-kit-1994-microbial-genome-project#:~:text=The%20DOE%20began%20a%20Microbial,bountiful%20microbial%20resources%20on%20Earth. Publication: https://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-13-S8-S4


Metrics

 The sequenced genome of Sneathia amnii has a size of 1.34 Mb with 110 overlapping genes (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3535699/). Researchers have not yet found what the overlapping genes exactly code for. Sneathia amnii’s percent GC is somewhere around 28% (Eisenberg et al., 2018). S. amnii contains 1,329 protein encoding genes. Analysis of S. amnii’s genome revealed it had a circular genome (Eisenberg et al., 2018). An interesting feature of S. amnii is that its compact genome is the smallest in the Fusocateriaceae family, but the size does not affect the length of the DNA sequences between genes.

Relevance

 It was decided that the species Leptotrichia sanguinegens should be assigned to a different genus based on phylogenetic and phenotypic analyses. The genus of the bacteria described was Sneathia, so it seemed best fit to be named Sneathia sanguinegens. Similarly, another novel species that was closely related to Snethia sanguinegens was taken from amniotic fluid. Initially, the bacteria was published as Leptotrichia amnionii. There was no valid species or type strain designated but the 16S rDNA phylogenetic analysis indicated that "L. amnionii" fit the description of the genus Sneathia better, which was the reason this gene was sequenced (Harwich et al., 2012). The vaginal isolate was reclassified to the genus Sneathia and designated Sneathia amnii sp. nov. The culturing, cloning and identification of S. amnii was done at Virginia Commonwealth University as part of the Vaginal Human Microbiome Project.

 The genome tells us that presently, Sneathia amnii displays the smallest genome out of the Fusobacteriaceae family. Despite the genome of S. amnii being small, its gene or coding density is higher than the average gene density of other bacteria in the Fusobacteriaceae family. Research found that the difference in size of S. amnii and its close relatives was due to the composition, or number of base pairs. This is due to of all its overlapping genes. The number is somewhere around 110 or more overlapping genes (Eisenberg et al., 2018)! It has been proven that S. amnii is susceptible to selective pressures of the environment just from the sequencing. This attributes to the high cost of the genome size and replication resulting in the compact genome. Of course, there’s a reason behind it! The logic behind this super compact genome is that the ability to replicate DNA, which is essential to function, can be kept while other abilities like cell motility and cell signaling can be “sacrificed”. Sneathia is under pressure to reduce genetic capabilities to only what is absolutely necessary in order to benefit most from the host (Eisenberg et al., 2018). Harwich et al (2012) found that 66% of Sneathia’s genes had putative function, meaning that there are similar functions shared between a lot of these genes. This is an interesting feature because the function and purpose of putative genes is not yet fully understood.


 Sneathi amnii’s resistance to metronidazole is important for its survival because it can continue its anerobic growth. Metronidazole is an antibiotic used to treat infections by the mechanism of stunting growth of bacteria it is used against (https://academic.oup.com/jac/article/73/2/265/4565576). It is the most common treatment for Gram-stain negative bacteria, so if it can resist and keep growing then it will be successful in carrying on the pathogenic processes (Eschenbach, 2007). S. amnii is given a form of “life insurance” through antibiotic resistance. If genes for the antibiotic resistance are carried by plasmids, or other genetic elements with transfer capability, it can be relayed to pathogenic bacteria and withstand the negative effects of antibiotics. These plasmids or other genetic elements with transfer can potentially spread into the bacterial community by horizontal gene transfer (Escudeiro et al., 2019).

Interesting Feature

Snethia amnii’s ability to damage fetuses comes from its production of cyotpathegonic toxin component A, or CptA (Gentille et al., 2020). CptA acts in a virulent way by lysing human red blood cells, leading to the damage of the fetal membrane’s cells. This is interesting because there is not much detail known about the virulence factor and mechanism of disease of S. amnii. It seems that the gene is cotranscribed along with a second gene that encodes a protein, similar to two-partner system transporters. Gram negative bacteria often use the two-partner secretion system to export hemolysins and other virulence factors. CptA contains 1,881 amino acids and weighs about 200 kDa. Cyotpathegonic toxin component A shows very little amino acid sequence homology to other known toxins. It performs its toxic actions by binding to the membranes of red blood cell and forming pores 2.0 to 3.0 nm long, resulting in cell lysis (Gentille et al., 2020).

References

1. Eisenberg, T., Glaser, S. P., Blom, J., & Kampfer, P. (2018, June 14). Sneathia. Retrieved November 06, 2020, from https://onlinelibrary-wiley-com.proxy-tu.researchport.umd.edu/doi/10.1002/9781118960608.gbm00773.pub2 2. Harwich Jr, M.D., Serrano, M.G., Fettweis, J.M., Alves, J.M., and Reimers, M.A. “Genomic sequence analysis and characterization of Sneathia amnii sp. nov.” BMC genomics. 2012. Volume 13. 3. Duployez, C., Le Guern, R., Faure, E., Wallet, F., and Loiez, C. “Sneathia amnii, an unusual pathogen in spondylitis: A case report”. Anerobe. 2020. Volume 66, 102277. 4. JGI GOLD: Project. (n.d.). Retrieved November 06, 2020, from https://gold.jgi.doe.gov/project?id=Gp0121048 5. Swidsinski, A., Mendling, W., Loening-Baucke, V., Ladhoff, A., Swidsinski, S., Hale, L. P., and Lochs, H. “Adherent biofilms in bacterial vaginosis”. Obstetrics and gynecology. 2012. 106(5 Pt 1). P. 1013–1023. https://doi.org/10.1097/01.AOG.0000183594.45524.d2 6. Smith, S.B. and Ravel, J. “The vaginal microbiota, host defence and reproductive physiology”. J Physiol. 2017. Volume 595. p. 451-463. https://doi.org/10.1113/JP271694 7. Ray, A. F., Peirce, S. C., Wilkes, A. R., and Carolan-Rees, G. “Vision Amniotic Leak Detector (ALD) to Eliminate Amniotic Fluid Leakage as a Cause of Vaginal Wetness in Pregnancy: A NICE Medical Technology Guidance”. Applied health economics and health policy. 2015. Volume13(5). p 445–456. https://doi.org/10.1007/s40258-015-0190-5 8. Wolrath, H., Forsum, U., Larsson, P. G., and Borén, H. “Analysis of bacterial vaginosis-related amines in vaginal fluid by gas chromatography and mass spectrometry”. Journal of clinical microbiology. 2001. Volume 39. p. 4026–4031. https://doi.org/10.1128/JCM.39.11.4026-4031.2001 9. The University of Maine. Carbohydrates [internet]. USA: The University of Maine. Available from: https://umaine.edu/carbohydrates/carbohydrate-digestion/fermentation/ESC 10. Eschenbach, D.A. “Bacterial Vaginosis: Resistance, Recurrence, and/or Reinfection?” Clinical Infectious Diseases. 2007. Volume 44. p. 220–221. https://doi.org/10.1086/509584 11. Gentile, G. L., Rupert, A. S., Carrasco, L. I., Garcia, E.M., Kumar, N. G., Walsh, S.W. and Kimberly, K. “Identification of a Cytopathogenic Toxin from Sneathia amnii” Jefferson Journal of Bacteriology. 2020. Volume 202 (13). e00162-20. doi: 10.1128/JB.00162-20 12. Deutscher, J., Francke, C., and Postma, P.W. “How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria”. Microbiology and Molecular Biology Reviews. 2008. Volume 70 (4). p 939-1031. doi: 10.1128/MMBR.00024-06 13. Fettweis, J.M., Serrano, M.G., Brooks, J.P. et al. “The vaginal microbiome and preterm birth”. 2019. Nature Medicine. Volume 25, p. 1012–102. doi.org/10.1038/s41591-019-0450-2 14. MicrobeWiki. Lactobacillus crispatus. United States: MicrobeWiki; 2017. Available from: https://microbewiki.kenyon.edu/index.php/Lactobacillus_crispatus 15. Witkin, S.S., and Linhares, I.M. “Why do lactobacilli dominate the human vaginal microbiota?” BJOG. 2017. Volume 124. p. 606– 611. 16. MicrobeWiki. Gardenerella vaginalis. United States: MicrobeWiki; 2010. Available from: https://microbewiki.kenyon.edu/index.php/Gardenerella_vaginalis 17. MicrobeWiki. Prevotella. United States: MicrobeWiki; 2010. Available from: https://microbewiki.kenyon.edu/index.php/Prevotella 18. MicrobeWiki. Peptostreptococcus anaerobius. United States: MicrobeWiki; 2020. Available from: https://microbewiki.kenyon.edu/index.php/Peptostreptococcus_anaerobius 19. MicrobeWiki. Ureaplasma urelyticum. United States: MicrobeWiki; 2010. Available from: https://microbewiki.kenyon.edu/index.php/Ureaplasma_urealyticum 20. MicrobeWiki. Mycoplasma hominis. United States: MicrobeWiki; 2013. Available from: https://microbewiki.kenyon.edu/index.php/Mycoplasma_hominis 21. Aldunate, M., Srbinovski, D., Hearps, A., Latham, C., Ramsland, P., Gugasyan, R., Cone, R., and Tachedjian, Gilda. “Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis”. Frontiers in physiology. 2015. Volume 6. p. 164. doi:10.3389/fphys.2015.00164.

Edited by Maleeka Raymond, a @MicrobialTowson student of Dr. Anne M. Estes at Towson University. Template adapted from templates by Angela Kent, University of Illinois at Urbana-Champaign and James W. Brown, Microbiology, NC State University.

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