Veillonella catalase protects the growth of Fusobacterium nucleatum in microaerophilic and Streptococcus gordonii-resident environments

Applied and Environmental Microbiology

Volumn 83, Issue 19, 2017, Pages

  Zhou, Peng ^a,d   Li, Xiaoli ^a   Huang, I Hsiu ^b   Qi, Fengxia ^a,c  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Anaerobes; Fusobacterium nucleatum; Oxidative stress; Streptococcus gordonii; Transformable strain; Veillonellae

Indexed keywords

BACTERIA; BIOFILMS; GENE EXPRESSION; GENES; OXIDATIVE STRESS;

ANAEROBES; ECOLOGICAL FUNCTIONS; FUSOBACTERIUM NUCLEATUM; MICROAEROPHILIC CONDITION; MULTI-SPECIES COMMUNITIES; MUTANS STREPTOCOCCI; STREPTOCOCCUS GORDONII; VEILLONELLAE;

ECOLOGY;

ANOXIC CONDITIONS; ANTAGONISM; BACTERIUM; BIOFILM; BIOTRANSFORMATION; ENZYME; EXPERIMENTAL STUDY; GENE EXPRESSION; GROWTH; MICROBIAL COMMUNITY; MUTUALISM; OXIDATIVE STRESS; PATHOGENICITY;

FUSOBACTERIUM NUCLEATUM; STREPTOCOCCUS GORDONII; VEILLONELLA; VEILLONELLA ATYPICA; VEILLONELLA PARVULA;

BACTERIAL PROTEIN; CATALASE; HYDROGEN PEROXIDE;

BIODIVERSITY; ENZYMOLOGY; FUSOBACTERIUM NUCLEATUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; MOUTH; STREPTOCOCCUS GORDONII; VEILLONELLA;

BACTERIAL PROTEINS; BIODIVERSITY; CATALASE; FUSOBACTERIUM NUCLEATUM; HUMANS; HYDROGEN PEROXIDE; MOUTH; STREPTOCOCCUS GORDONII; VEILLONELLA;

EID: 85029555945     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01079-17     Document Type: Article

References (49)

1. Huang R, Li M, Gregory RL. 2011. Bacterial interactions in dental biofilm. Virulence 2:435-444. https://doi.org/10.4161/viru.2.5.16140
2. Hajishengallis G, Lamont RJ. 2012. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27:409-419. https:// doi.org/10.1111/j.2041-1014.2012.00663.x
3. Kolenbrander PE, Palmer RJ, Jr, Periasamy S, Jakubovics NS. 2010. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8:471-480. https://doi.org/10.1038/nrmicro2381
4. Kolenbrander PE, Palmer RJ, Jr, Rickard AH, Jakubovics NS, Chalmers NI, Diaz PI. 2006. Bacterial interactions and successions during plaque development. Periodontol 2000 42:47-79. https://doi.org/10.1111/j.1600-0757.2006.00187.x
5. Diaz PI, Chalmers NI, Rickard AH, Kong C, Milburn CL, Palmer RJ, Jr, Kolenbrander PE. 2006. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl Environ Microbiol 72:2837-2848. https://doi.org/10.1128/AEM.72.4.2837-2848.2006
6. Zhou P, Li X, Qi F. 2016. Identification and characterization of a heme biosynthesis locus in Veillonella. Microbiology 162:1735-1743. https:// doi.org/10.1099/mic.0.000366
7. Marsh PD. 2006. Dental plaque as a biofilm and a microbial community-implications for health and disease. BMC Oral Health 6(Suppl 1):S14
8. Marsh PD. 1999. Microbiologic aspects of dental plaque and dental caries. Dent Clin North Am 43:599-614, v-vi
9. Marsh PD, Bradshaw DJ. 1995. Dental plaque as a biofilm. J Ind Microbiol 15:169-175. https://doi.org/10.1007/BF01569822
10. Okahashi N, Nakata M, Sumitomo T, Terao Y, Kawabata S. 2013. Hydrogen peroxide produced by oral streptococci induces macrophage cell death. PLoS One 8:e62563. https://doi.org/10.1371/journal.pone.0062563
11. Chen L, Ge X, Dou Y, Wang X, Patel JR, Xu P. 2011. Identification of hydrogen peroxide production-related genes in Streptococcus sanguinis and their functional relationship with pyruvate oxidase. Microbiology 157:13-20. https://doi.org/10.1099/mic.0.039669-0
12. Coykendall AL. 1989. Classification and identification of the viridans streptococci. Clin Microbiol Rev 2:315-328. https://doi.org/10.1128/CMR.2.3.315
13. Kreth J, Zhang Y, Herzberg MC. 2008. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol 190:4632-4640. https://doi.org/ 10.1128/JB.00276-08
14. Hughes CV, Roseberry CA, Kolenbrander PE. 1990. Isolation and characterization of coaggregation-defective mutants of Veillonella atypica. Arch Oral Biol 35(Suppl):123S-125S
15. Liu J, Wu C, Huang IH, Merritt J, Qi F. 2011. Differential response of Streptococcus mutans towards friend and foe in mixed-species cultures. Microbiology 157:2433-2444. https://doi.org/10.1099/mic.0.048314-0
16. Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, Leys EJ, Paster BJ. 2008. Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46:1407-1417. https://doi.org/10.1128/JCM.01410-07
17. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. 2005. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721-5732. https://doi.org/10.1128/JCM.43.11.5721-5732.2005
18. Becker MR, Paster BJ, Leys EJ, Moeschberger ML, Kenyon SG, Galvin JL, Boches SK, Dewhirst FE, Griffen AL. 2002. Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001-1009. https://doi.org/10.1128/JCM.40.3.1001-1009.2002
19. Rogosa M. 1964. The genus Veillonella. I. General cultural, ecological, and biochemical considerations. J Bacteriol 87:162-170
20. Hughes CV, Kolenbrander PE, Andersen RN, Moore LV. 1988. Coaggregation properties of human oral Veillonella spp.: relationship to colonization site and oral ecology. Appl Environ Microbiol 54:1957-1963
21. Chalmers NI, Palmer RJ, Jr, Cisar JO, Kolenbrander PE. 2008. Characterization of a Streptococcus sp.-Veillonella sp. community micromanipulated from dental plaque. J Bacteriol 190:8145-8154. https://doi.org/10.1128/JB.00983-08
22. Periasamy S, Kolenbrander PE. 2010. Central role of the early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. J Bacteriol 192:2965-2972. https://doi.org/10.1128/JB.01631-09
23. Zhou P, Liu J, Merritt J, Qi F. 2015. A YadA-like autotransporter, Hag1 in Veillonella atypica is a multivalent hemagglutinin involved in adherence to oral streptococci, Porphyromonas gingivalis, and human oral buccal cells. Mol Oral Microbiol 30:269-279. https://doi.org/10.1111/omi.12091
24. Kolenbrander PE, Andersen RN, Moore LV. 1989. Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect Immun 57:3194-3203
25. Signat B, Roques C, Poulet P, Duffaut D. 2011. Fusobacterium nucleatum in periodontal health and disease. Curr Issues Mol Biol 13:25-36
26. Diaz PI, Zilm PS, Rogers AH. 2002. Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxidedepleted environments. Microbiology 148:467-472. https://doi.org/10.1099/00221287-148-2-467
27. Kraus FW, Nickerson JF, Perry WI, Walker AP. 1957. Peroxide and peroxidogenic bacteria in human saliva. J Bacteriol 73:727-735
28. Zhou P, Li X, Qi F. 2015. Establishment of a counter-selectable markerless mutagenesis system in Veillonella atypica. J Microbiol Methods 112: 70-72. https://doi.org/10.1016/j.mimet.2015.03.010
29. Liu J, Xie Z, Merritt J, Qi F. 2012. Establishment of a tractable genetic transformation system in Veillonella spp. Appl Environ Microbiol 78: 3488-3491. https://doi.org/10.1128/AEM.00196-12
30. Spolarics Z, Wu JX. 1997. Role of glutathione and catalase in H2O2 detoxification in LPS-activated hepatic endothelial and Kupffer cells. Am J Physiol 273:G1304-G1311
31. Das D, Bishayi B. 2009. Staphylococcal catalase protects intracellularly survived bacteria by destroying H2O2 produced by the murine peritoneal macrophages. Microb Pathog 47:57-67. https://doi.org/10.1016/j.micpath.2009.04.012
32. Liu J, Merritt J, Qi F. 2011. Genetic transformation of Veillonella parvula. FEMS Microbiol Lett 322:138-144. https://doi.org/10.1111/j.1574-6968.2011.02344.x
33. Zhou P, Xie G, Li X, Liu J, Qi F. 2017. Complete genome sequence of Veillonella atypica OK5, the first transformable strain in the species. Genome Announc 5(22):e00391-17. https://doi.org/10.1128/genomeA.00391-17
34. Zhou P, Liu L, Tong H, Dong X. 2012. Role of operon aaoSo-mutT in antioxidant defense in Streptococcus oligofermentans. PLoS One 7:e38133. https://doi.org/10.1371/journal.pone.0038133
35. Farr SB, Kogoma T. 1991. Oxidative stress responses in Escherichia coli and Salmonella Typhimurium. Microbiol Rev 55:561-585
36. Yesilkaya H, Kadioglu A, Gingles N, Alexander JE, Mitchell TJ, Andrew PW. 2000. Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect Immun 68: 2819-2826. https://doi.org/10.1128/IAI.68.5.2819-2826.2000
37. Lumppio HL, Shenvi NV, Summers AO, Voordouw G, Kurtz DM, Jr. 2001. Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris: a novel oxidative stress protection system. J Bacteriol 183:101-108. https://doi.org/10.1128/JB.183.1.101-108.2001
38. Lynch MC, Kuramitsu HK. 1999. Role of superoxide dismutase activity in the physiology of Porphyromonas gingivalis. Infect Immun 67: 3367-3375
39. Jenney FE, Jr, Verhagen MF, Cui X, Adams MW. 1999. Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286:306-309. https://doi.org/10.1126/science.286.5438.306
40. Sztukowska M, Bugno M, Potempa J, Travis J, Kurtz DM, Jr. 2002. Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis. Mol Microbiol 44:479-488. https://doi.org/10.1046/j.1365-2958.2002.02892.x
41. Barré O, Mourlane F, Solioz M. 2007. Copper induction of lactate oxidase of Lactococcus lactis: a novel metal stress response. J Bacteriol 189: 5947-5954. https://doi.org/10.1128/JB.00576-07
42. Rodriguez R, Redman R. 2005. Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci U S A 102:3175-3176. https://doi.org/10.1073/pnas.0500367102
43. 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:e0143898. https://doi.org/ 10.1371/journal.pone.0143898
44. Chen T, Yu WH, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE. 2010. The Human Oral Microbiome Database: a Web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) https://doi.org/10.1093/database/baq013
45. Coulter ED, Kurtz DM, Jr. 2001. A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris: catalytic electron transfer to rubrerythrin and two-iron superoxide reductase. Arch Biochem Biophys 394:76-86. https://doi.org/10.1006/abbi.2001.2531
46. Periasamy S, Kolenbrander PE. 2009. Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleatum and Veillonella species in saliva. Infect Immun 77:3542-3551. https://doi.org/10.1128/IAI.00345-09
47. He X, Wu C, Yarbrough D, Sim L, Niu G, Merritt J, Shi W, Qi F. 2008. The cia operon of Streptococcus mutans encodes a unique component required for calcium-mediated autoregulation. Mol Microbiol 70:112-126. https://doi.org/10.1111/j.1365-2958.2008.06390.x
48. Pakula R, Walczak W. 1963. On the nature of competence of transformable streptococci. J Gen Microbiol 31:125-133. https://doi.org/10.1099/ 00221287-31-1-125
49. Loesche WJ. 1986. Role of Streptococcus mutans in human dental decay. Microbiol Rev 50:353-380