Description of gen. nov., sp. nov., a high-molecular-weight polycyclic aromatic hydrocarbon-degrading bacterium within the class , and proposal of ord. nov. and fam. nov. Free

Abstract

The bacterial strain TR3.2 was isolated from aerobic bioreactor-treated soil from a polycyclic aromatic hydrocarbon (PAH)-contaminated site in Salisbury, NC, USA. Strain TR3.2 was identified as a member of ‘Pyrene Group 2’ or ‘PG2’, a previously uncultivated cluster of organisms associated with the degradation of high-molecular-weight PAHs by stable-isotope probing. Based on its 16S rRNA gene sequence, the strain was classified as a member of the class but possessed only 90.5 % gene identity to its closest described relative, strain Bath. Strain TR3.2 grew on the PAHs pyrene, phenanthrene, anthracene, benz[]anthracene and fluorene, as well as the azaarene carbazole, and could additionally metabolize a limited number of organic acids. Optimal growth occurred aerobically under mesophilic temperature, neutral pH and low salinity conditions. Strain TR3.2 was catalase and oxidase positive. Predominant fatty acids were C cyclo and C. Genomic G+C content of the single chromosome was 67.79 mol% as determined by complete genome sequencing. Due to the high sequence divergence from any cultivated species and its unique physiological properties compared to its closest relatives, strain TR3.2 is proposed as a representative of a novel order, family, genus and species within the class , for which the name gen. nov., sp. nov. is proposed. The associated order and family are therefore proposed as ord. nov. and fam. nov. The type strain of the species is TR3.2 (=ATCC TSD-58=DSM 103040).

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2017-04-01
2024-03-29
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References

  1. Singleton DR, Sangaiah R, Gold A, Ball LM, Aitken MD. Identification and quantification of uncultivated Proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environ Microbiol 2006; 8:1736–1745 [View Article][PubMed]
    [Google Scholar]
  2. Jones MD, Crandell DW, Singleton DR, Aitken MD. Stable-isotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. Environ Microbiol 2011; 13:2623–2632 [View Article][PubMed]
    [Google Scholar]
  3. Jones MD, Singleton DR, Carstensen DP, Powell SN, Swanson JS et al. Effect of incubation conditions on the enrichment of pyrene-degrading bacteria identified by stable-isotope probing in an aged, PAH-contaminated soil. Microb Ecol 2008; 56:341–349 [View Article][PubMed]
    [Google Scholar]
  4. Singleton DR, Hunt M, Powell SN, Frontera-Suau R, Aitken MD. Stable-isotope probing with multiple growth substrates to determine substrate specificity of uncultivated bacteria. J Microbiol Methods 2007; 69:180–187 [View Article][PubMed]
    [Google Scholar]
  5. Dunlevy SR, Singleton DR, Aitken MD. Biostimulation reveals functional redundancy of anthracene-degrading bacteria in polycyclic aromatic hydrocarbon-contaminated soil. Environ Eng Sci 2013; 30:697–705 [View Article][PubMed]
    [Google Scholar]
  6. Li D, Midgley DJ, Ross JP, Oytam Y, Abell GC et al. Microbial biodiversity in a Malaysian oil field and a systematic comparison with oil reservoirs worldwide. Arch Microbiol 2012; 194:513–523 [View Article][PubMed]
    [Google Scholar]
  7. Liu R, Zhang Y, Ding R, Li D, Gao Y et al. Comparison of archaeal and bacterial community structures in heavily oil-contaminated and pristine soils. J Biosci Bioeng 2009; 108:400–407 [View Article][PubMed]
    [Google Scholar]
  8. Païssé S, Goñi-Urriza M, Coulon F, Duran R. How a bacterial community originating from a contaminated coastal sediment responds to an oil input. Microb Ecol 2010; 60:394–405 [View Article][PubMed]
    [Google Scholar]
  9. Tauler M, Vila J, Nieto JM, Grifoll M. Key high molecular weight PAH-degrading bacteria in a soil consortium enriched using a sand-in-liquid microcosm system. Appl Microbiol Biotechnol 2016; 100:3321–3336 [View Article][PubMed]
    [Google Scholar]
  10. Bai Y, Sun Q, Sun R, Wen D, Tang X. Bioaugmentation and adsorption treatment of coking wastewater containing pyridine and quinoline using zeolite-biological aerated filters. Environ Sci Technol 2011; 45:1940–1948 [View Article][PubMed]
    [Google Scholar]
  11. Militon C, Boucher D, Vachelard C, Perchet G, Barra V et al. Bacterial community changes during bioremediation of aliphatic hydrocarbon-contaminated soil. FEMS Microbiol Ecol 2010; 74:669–681 [View Article][PubMed]
    [Google Scholar]
  12. Kim JS, Crowley DE. Microbial diversity in natural asphalts of the Rancho La Brea tar pits. Appl Environ Microbiol 2007; 73:4579–4591 [View Article][PubMed]
    [Google Scholar]
  13. Handley KM, Verberkmoes NC, Steefel CI, Williams KH, Sharon I et al. Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community. ISME J 2013; 7:800–816 [View Article][PubMed]
    [Google Scholar]
  14. Gihring TM, Moser DP, Lin L-H, Davidson M, Onstott TC et al. The distribution of microbial taxa in the subsurface water of the Kalahari Shield, South Africa. Geomicrobiol J 2006; 23:415–430 [View Article]
    [Google Scholar]
  15. Liu R, Yu Z, Zhang H, Yang M, Shi B et al. Diversity of bacteria and mycobacteria in biofilms of two urban drinking water distribution systems. Can J Microbiol 2012; 58:261–270 [View Article][PubMed]
    [Google Scholar]
  16. Xia N, Xia X, Zhu B, Zheng S, Zhuang J. Bacterial diversity and community structure in the sediment of the middle and lower reaches of the Yellow River, the largest turbid river in the world. Aquat Microb Ecol 2013; 71:43–55 [View Article]
    [Google Scholar]
  17. Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H et al. Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2004; 2:e303 [View Article][PubMed]
    [Google Scholar]
  18. Whittenbury R, Phillips KC, Wilkinson JF. Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 1970; 61:205–218 [View Article][PubMed]
    [Google Scholar]
  19. Singleton DR, Richardson SD, Aitken MD. Pyrosequence analysis of bacterial communities in aerobic bioreactors treating polycyclic aromatic hydrocarbon-contaminated soil. Biodegradation 2011; 22:1061–1073 [View Article][PubMed]
    [Google Scholar]
  20. Kojima H, Fukui M. Sulfuritalea hydrogenivorans gen. nov., sp. nov., a facultative autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 2011; 61:1651–1655 [View Article][PubMed]
    [Google Scholar]
  21. Corteselli EM, Aitken MD, Singleton DR. Rugosibacter aromaticivorans gen. nov., sp. nov., a bacterium within the family Rhodocyclaceae, isolated from contaminated soil, capable of degrading aromatic compounds. Int J Syst Evol Microbiol 2017; 67:311–318 [View Article][PubMed]
    [Google Scholar]
  22. Singleton DR, Dickey AN, Scholl EH, Wright FA, Aitken MD. Complete genome sequence of a bacterium representing a deep uncultivated lineage within the Gammaproteobacteria associated with the degradation of polycyclic aromatic hydrocarbons. Genome Announc 2016; 4:e01086-16 [View Article][PubMed]
    [Google Scholar]
  23. Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A. A rapid and easy method for the detection of microbial cellulases on agar plates using Gram's iodine. Curr Microbiol 2008; 57:503–507 [View Article][PubMed]
    [Google Scholar]
  24. Kanaly RA, Harayama S. Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microb Biotechnol 2010; 3:136–164 [View Article][PubMed]
    [Google Scholar]
  25. Schell MA. Cloning and expression in Escherichia coli of the naphthalene degradation genes from plasmid NAH7. J Bacteriol 1983; 153:822–829[PubMed]
    [Google Scholar]
  26. Richardson SD, Lebron BL, Miller CT, Aitken MD. Recovery of phenanthrene-degrading bacteria after simulated in situ persulfate oxidation in contaminated soil. Environ Sci Technol 2011; 45:719–725 [View Article][PubMed]
    [Google Scholar]
  27. Singleton DR, Ramirez LG, Aitken MD. Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading Acidovorax strain. Appl Environ Microbiol 2009; 75:2613–2620 [View Article][PubMed]
    [Google Scholar]
  28. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids MIDI Technical Note 101 2001 www.microbialid.com/PDF/TechNote_101.pdf
    [Google Scholar]
  29. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990; 13:128–130 [View Article]
    [Google Scholar]
  30. Tindall BJ. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 1990; 66:199–202 [View Article]
    [Google Scholar]
  31. Tindall BJ, Sikorski J, Smibert RM, Kreig NR. Phenotypic characterization and the principles of comparative systematics. In Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM. et al. (editors) Methods for General and Molecular Microbiology Washington, DC: ASM Press; 2007 pp. 330–393
    [Google Scholar]
  32. Muyzer G, Sorokin DY, Mavromatis K, Lapidus A, Clum A et al. Complete genome sequence of "Thioalkalivibrio sulfidophilus" HL-EbGr7. Stand Genomic Sci 2011; 4:23–35 [View Article][PubMed]
    [Google Scholar]
  33. Slobodkina GB, Baslerov RV, Novikov AA, Viryasov MB, Bonch-Osmolovskaya EA et al. Inmirania thermothiophila gen. nov., sp. nov., a thermophilic, facultatively autotrophic, sulfur-oxidizing gammaproteobacterium isolated from a shallow-sea hydrothermal vent. Int J Syst Evol Microbiol 2016; 66:701–706 [View Article][PubMed]
    [Google Scholar]
  34. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  35. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73:5261–5267 [View Article][PubMed]
    [Google Scholar]
  36. Martin F, Torelli S, Le Paslier D, Barbance A, Martin-Laurent F et al. Betaproteobacteria dominance and diversity shifts in the bacterial community of a PAH-contaminated soil exposed to phenanthrene. Environ Pollut 2012; 162:345–353 [View Article][PubMed]
    [Google Scholar]
  37. Bowman JP. Order VII. Methylococcales ord. nov. In Brenner DJ, Staley JT. (editors) Bergey's Manual of Systematic Bacteriology. Volume 2: The Proteobacteria Part B: The Gammaproteobacteria New York: Springer; 2005
    [Google Scholar]
  38. Hoefman S, Van der Ha D, Iguchi H, Yurimoto H, Sakai Y et al. Methyloparacoccus murrellii gen. nov., sp. nov., a methanotroph isolated from pond water. Int J Syst Evol Microbiol 2014; 64:2100–2107 [View Article][PubMed]
    [Google Scholar]
  39. Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE et al. Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov., and Thioalkalivibrio denitrificancs sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 2001; 51:565–580 [View Article][PubMed]
    [Google Scholar]
  40. Imhoff JF. Order I. Chromatiales ord. nov. In Brenner DJ, Staley JT. (editors) Bergey's Manual of Systematic Bacteriology. Volume 2: The Proteobacteria Part B: The Gammaproteobacteria New York: Springer; 2005
    [Google Scholar]
  41. Campbell MA, Chain PS, Dang H, El Sheikh AF, Norton JM et al. Nitrosococcus watsonii sp. nov., a new species of marine obligate ammonia-oxidizing bacteria that is not omnipresent in the world's oceans: calls to validate the names 'Nitrosococcus halophilus' and 'Nitrosomonas mobilis'. FEMS Microbiol Ecol 2011; 76:39–48 [View Article][PubMed]
    [Google Scholar]
  42. Klotz MG, Arp DJ, Chain PS, El-Sheikh AF, Hauser LJ et al. Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl Environ Microbiol 2006; 72:6299–6315 [View Article][PubMed]
    [Google Scholar]
  43. Narasingarao P, Häggblom MM. Sedimenticola selenatireducens, gen. nov., sp. nov., an anaerobic selenate-respiring bacterium isolated from estuarine sediment. Syst Appl Microbiol 2006; 29:382–388 [View Article][PubMed]
    [Google Scholar]
  44. Mori K, Suzuki K, Urabe T, Sugihara M, Tanaka K et al. Thioprofundum hispidum sp. nov., an obligately chemolithoautotrophic sulfur-oxidizing gammaproteobacterium isolated from the hydrothermal field on Suiyo Seamount, and proposal of Thioalkalispiraceae fam. nov. in the order Chromatiales. Int J Syst Evol Microbiol 2011; 61:2412–2418 [View Article][PubMed]
    [Google Scholar]
  45. Takai K, Miyazaki M, Hirayama H, Nakagawa S, Querellou J et al. Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ Microbiol 2009; 11:1983–1997 [View Article][PubMed]
    [Google Scholar]
  46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25:4876–4882 [View Article][PubMed]
    [Google Scholar]
  47. Cummings MP, Hancock JM, Zvelebil MJ. PAUP* (phylogenetic analysis using parsimony (and other methods)). Dictionary of Bioinformatics and Computational Biology Hoboken, NJ: John Wiley & Sons, Ltd; 2004
    [Google Scholar]
  48. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article][PubMed]
    [Google Scholar]
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