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Saeed Jami Bench A 22/09/16 ^[1]

Classification

Higher order taxa

Bacteria – Firmicutes – Negativicutes – Selenomonadales – Veillonellaceae – Veillonella

Species

Veillonella parvula

Type Strain: Prevot Te 3, ATCC 10790 T, CCUG 5123 T, NCTC 11810 T

Description and significance

French biologist Adrein Veillon, whom the species is named after, first discovered the species in 1898^[3][4]. Veillonella parvula is a gram negative bacteria found in microenvironments of the human body, commonly described in human intestinal, oral and vaginal microflora^[5][6][7]. Despite being part of the Firmicutes phyla, majority of which are gram positive, Veillonella has a peculiar gram negative cell wall known of the Negativicutes class. V. parvula essentially anaerobic and auxotrophic; it is also lactate fermenting, cocci shaped^[2][5][8][9] and small in size at 0.3-0.5 μm^[2].

With great association with other genera, particularly with Streptococcus^[10], Veillonella is incapable of metabolising common sugars but will ferment other energy sources^[11]. V. parvula binds to the surface of other fermenting bacteria and metabolises/ferments lactate, which is commonly released as an anaerobic respiration by-product in bacteria^[10][12]. This is beneficiary as it removes completion for resource acquisition and also, coaggregation of Veillonella and certain Streptococcus species promotes the formation of biofilm^[10]; although this is subject to preferential treatment between species^[10]. Both of whom are known as early stage colonisers within oral plaque communities^[12].

Neither pathogenic or beneficial to human hosts, this species is important to understand due to its role within human health and its importance in microbial community composition, specifically within oral plaques. Although, V. parvula may be an opportunistic pathogen, it is quite uncommon but due to the severity of infection, this warrants research and study within this aspect.

Genome structure

Fully sequenced and analysed in 2009 by Gronow et al.^[2], the type strain ATCC 10790 of Veillonella parvula has a circular genome of 2.13 Mbp in length with about one gene per 1.1 kbp for density of protein coding genes. 1920 genes are within the genome and 97% of these are protein coding with the remainder being RNA coding; 0.78% of which were predicted as being pseudogenes. There have been no extrachromosomal elements detected and the genome contained a GC content of 39%. Common within the Firmicutes phylum, V. parvula’s genome size is normal while the protein coding density is low^[14][15] compared to average bacterial properties^[13].

Cell structure and metabolism

A member of the Negativicutes class of bacteria, V. parvula do not stain gram positive like other species of the Firmicutes phylum. It stains gram negative^{[2][4][9][17]} and has a cell wall composition that is common to gram negative bacteria, a lipopolysaccharide coated outer membrane, a thin peptidoglycan layer, and an inner cytoplasmic membrane^[18][19]. The thin peptidoglycan layer characteristically contains two diamine compounds, cardaverine and putrescine, to maintain the peptidoglycan layer and cell wall integrity^[20]. Compromise of these two diamine compounds results in cell death. The cell wall also contains the plamalogens plasmenylthanolamine and plasmenylserine, located in the cytoplasmic membrane, which regulates the fluidity of the membrane and specific for V. parvula^[17].

The inability of the Veillonella genus to metabolise glucose is partially explained by its lack of hexokinase, an enzyme required for the first step of glycolysis^[11]. Rogosa et al.^[11] has shown the rest of the glycolysis pathway in the Veillonella genus is function. This suggest that the pathway could instead be a viable route for gluconeogenesis, ending in the production of glucose-6-phosphate.

Due to the inability to metabolism glucose, V. parvula utilises lactate, malate, and formate as energy sources, which are metabolised anaerobically producing acetate, carbon dioxide, hydrogen gas, and propionate. Lactate and malate, common by-products of fermentation, are plentiful in the oral and gastrointestinal microbiomes, which are populated by many fermentative bacteria. Additionally, V. parvula is capable of taking up succinate as a co-factor to improve growth rate^[21]. ~50% of lactate that V. parvula metabolises is oxidised to pyruvate and then degraded to acetate yielding one ATP. The rest is converted to succinate, malate and formate are intermediates, and then degraded to propionate by methlmalonyldecarboxylase (MMD). No ATP is released from this reaction, but energy produced by the membrane bound MMD catalysing this reaction is usead to generate electrochemical sodium gradients across the cytoplasmic membrane^[16]. Thus, energy that would have been used to maintain this electrochemical gradient can be redirected within the cell. This explains why growth rates increase when succinate is taken up in conjunction with lactate/malate/formate^[21].

Ecology

V. parvula appears to have a commensal relationship with humans whilst it has numerous interactions with other bacteria of the microbiome, these bacteria may in turn interact with the human host^[12]. The Veillonella genus has higher growth rates when partnered with lactate producing bacteria. Partnerships can be formed with Actinomyces oris, Porphyromonas gingervalis^[22], and any of the Streptococcus species^[12]. Interestingly, both partners have a higher growth rate together than alone. The specific Veillonella and partner species influences growth rate in addition to biofilm production^[10]. Perisamy^[12] described that in complex microbiomes, containing bacteria that Veillonella can partner with, inhibited the increased growth observed when Veillonella and a single partner bacteria are cultured together. This suggests that the Veillonella genus has high specificity for the species it interacts with for efficient utilisation of resources. Because of this and its role as an early plaque coloniser, that the Veillonella genus has an important role in the plaque community where it can dictate which of later plaque colonising species will have a greater abundance within the plaque. V. parvula can induce greater growth and biofilm production in various Streptococcus mutants and sanguinus^[10]. It has been associated with both healthy^[23][24] and unhealthy plaque communities^[25].

Pathology

V. parvula is a well-known species of the oral cavity microbiome. It does not appear to be associated with endodontitis or dental caries while its association with gingivitis is contentious^[26][27]. Outside of the oral cavity V. parvula has been found to cause osteomyelitis^[28], sepsis, bacteraemia^[29][30][31], spondylodiscitis^[32][33], urinary tract infection^[34] and endocarditis^[35]. However, instances of these infections are rare in healthy patients and in most cases the patient is immunocompromised through diabetes, HIV, old age, pregnancy, or recessive disorders. V. parvula is rarely the primary or sole cause of disease with many polymicrobial infections likely to have Veillonella present, this is not surprising become of its biofilm generation and multispecies interactions.

Application to biotechnology

There is little research into targeted pharmacotherapy of V. parvula due to its typically being non-pathogenic. V. parvula is a good model organism due to its high abundance in the oral cavity and it being the best understood of Veillonella species. Because it is not a good model of gram negative bacteria with better models available (Pseudomonas aeruginosa), V. parvula is not used. Attempts have been made to develop better research technics and technologies for the study of the Veillonella genus. Liu et al.^[37] investigated transformation techniques specific for V. parvula, aiming to better understand Veillonellaceae biology. A 1975 publication showed fluoresce of Veillonella can be induced by long wave ultraviolet light^[38], a useful technique for identifying species of the Veillonella genus within the microbiome.

Current research

V. parvula research is currently focusing on metagenomics studies of the oral cavity ^{[39][40][41][42][43]} in the context of the microbiome as a whole. Other research has investigated its role, in conjunction with other microbes, in disease and its unstudied genus. A metagenomics study by Cuthbertson et al. 2016^[45], illuminated the properties and composition of the notoriously difficulty to study and complex microbiome in addition to proposing biomarkers to predict periods of acute and worsening cystic fibrosis. These periods, known as cystic fibrosis pulmonary exacerbations (CFPEs), were found to be preceded by decreases in the proportional abundance of V. parvula/rogosae and decreased P. melaninogenica/veroralis/histicola. The power of this study stemmed from its coverage of the stages of CFPEs, through a very high frequency of sampling from the lungs of patients. Further, the core ‘metacommunity’ of cystic fibrosis lung microbiota was identified and the dynamics of this community, particularly during CFPE treatment typically through broad spectrum anti-biotics, was eluded to.

References

1. MICR3004

2. 2.0 2.1 2.2 2.3 2.4 Gronow, S., Welnitz, S., Lapidus, A., Nolan, M., Ivanova, N., Glavina Del Rio, T., . . . Lucas, S. (2010). Complete genome sequence of Veillonella parvula type strain (Te3). Stand Genomic Sci, 2(1), 57-65. doi:10.4056/sigs.521107

3. List of prokaryotic names with standing in nomenclature

4. 4.0 4.1 Veillon A, Zuber MM. Recherches sur quelques microbes strictement anaérobies et leur rôle en pathologie. Arch Med Exp 1898; 10:517-545.

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8. http://www.genome.jp/dbget-bin/www_bget?vpr:Vpar_1247+vpr:Vpar_1248+vpr:Vpar_1762+vpr:Vpar_1763

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22. Periasamy, S., & Kolenbrander, P. E. (2009). Mutualistic Biofilm Communities Develop with Porphyromonas gingivalis and Initial, Early and Late Colonizers of Enamel. Journal of Bacteriology, 191(22), 8. doi:6804-6811

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28. Al-Otaibi, F. E., & Al-Mohizea, M. M. (2014). Non-vertebral Veillonella species septicemia and osteomyelitis in a patient with diabetes: a case report and review of the literature. Journal of Medical Case Reports, 8(365), 5. doi:10.1186/1752-1947-8-365

29. Yagihashi, Y., & Arakaki, Y. (2012). Acute pyelonephritis and secondary bacteraemia caused by Veillonella during pregnancy. BMJ Case Rep, 2012. doi:10.1136/bcr-2012-007364

30. Strach, M., Siedlar, M., Kowalczyk, D., Zembala, M., & Grodzicki, T. (2006). Sepsis caused by Veillonella parvula infection in a 17-year-old patient with X-linked agammaglobulinemia (Bruton's disease). J Clin Microbiol, 44(7), 2655-2656. doi:10.1128/JCM.00467-06

31. Arrosagary, P. M., Salas, C., Morales, M., Correas, M., Barros, J. M., & Cordon, M. L. (1987). Bilateral Abscessed Orchiepididymitis Associated with Sepsis Caused by Veillonella parvula and Clostridium perfringens: Case Report and Review of the Literature. Journal of Clinical Microbiology, 25(8), 2.

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42. Hirai, J., Yamagishi, Y., Kinjo, T., Hagihara, M., Sakanashi, D., Suematsu, H., . . . Mikamo, H. (2016). Osteomyelitis caused by Veillonella species: Case report and review of the literature. J Infect Chemother, 22(6), 417-420. doi:10.1016/j.jiac.2015.12.015

43. Edlund, A., Yang, Y., Yooseph, S., Hall, A. P., Nguyen, D. D., Dorrestein, P. C., . . . McLean, J. S. (2015). Meta-omics uncover temporal regulation of pathways across oral microbiome genera during in vitro sugar metabolism. ISME J, 9(12), 2605-2619. doi:10.1038/ismej.2015.72

44. Pustelny, C., Komor, U., Pawar, V., Lorenz, A., Bielecka, A., Moter, A., . . . Haussler, S. (2015). Contribution of Veillonella parvula to Pseudomonas aeruginosa-mediated pathogenicity in a murine tumor model system. Infect Immun, 83(1), 417-429. doi:10.1128/IAI.02234-14

45. 45.0 45.1 Cuthbertson, L., Rogers, G. B., Walker, A. W., Oliver, A., Green, L. E., Daniels, T. W., . . . van der Gast, C. J. (2016). Respiratory microbiota resistance and resilience to pulmonary exacerbation and subsequent antimicrobial intervention. ISME J, 10(5), 1081-1091. doi:10.1038/ismej.2015.198

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47. Zhou, P., Liu, J., Li, X., Takahashi, Y., & Qi, F. (2015). The Sialic Acid Binding Protein, Hsa, in Streptococcus gordonii DL1 also Mediates Intergeneric Coaggregation with Veillonella Species. PLoS One, 10(11), e0143898. doi:10.1371/journal.pone.0143898

48. Edlund, A., Liu, Q., Watling, M., To, T. T., Bumgarner, R. E., He, X., . . . McLean, J. S. (2016). High-Quality Draft Genome Sequence of Low-pH-Active Veillonella parvula Strain SHI-1, Isolated from Human Saliva within an In Vitro Oral Biofilm Model. Genome Announc, 4(1). doi:10.1128/genomeA.01684-15

This page is written by Saeed Jami for the MICR3004 course, Semester 2, 2016