1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 7

sp. nov., a deep-sea hydrothermal vent tube worm endobiont capable of dissimilatory anaerobic metalloid oxyanion reduction No Access

Abstract

A polyphasic taxonomic study was carried out on a Gram-stain-negative and rod-shaped strain, ER-Te-42B-Light, isolated from the tissue of a tube worm, , collected near a deep-sea hydrothermal vent of the Juan de Fuca Ridge in the Pacific Ocean. This bacterium was capable of performing anaerobic respiration using tellurite, tellurate, selenite and orthovanadate as terminal electron acceptors. While facultatively anaerobic, it could aerobically resist tellurite, selenite and orthovanadate up to 2000, 7000 and 10000 µg ml, respectively, reducing each oxide to elemental forms. Nearly complete 16S rRNA gene sequence similarity related the strain to , with 98.8 and 98.7 % similarity to and , respectively. The dominant fatty acids were C and C. The major polar lipids were phosphatidylethanolamine and phosphatidylglycerol and MK-7 was the predominant quinone. DNA G+C content was 42.5 mol%. Computation of average nucleotide identity and digital DNA–DNA hybridization values with the closest phylogenetic neighbours of ER-Te-42B-Light revealed genetic divergence at the species level, which was further substantiated by differences in several physiological characteristics. Based on the obtained results, this bacterium was assigned to the genus as a new species with the name sp. nov., type strain ER-Te-42B-Light (=VKM B-3580=DSM 113370).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): anaerobic respiration on metal(loid) oxides , hydrothermal vent , Juan de Fuca Ridge microbes , metal(loid) resistance , Shewanella metallivivens and tube worm symbiont
Funding
This study was supported by the:
  • Wilson Enhancement Fund for Applied Research In Science
    • Principle Award Recipient: JohnA Kyndt
  • University of Manitoba Faculty of Science Scholarship
    • Principle Award Recipient: VladimirYurkov
  • Slippery Rock University Department of Biology
    • Principle Award Recipient: ChrisMaltman
  • Slippery Rock University Faculty Student Research Grant
    • Principle Award Recipient: ChrisMaltman
  • University of Manitoba GETS
    • Principle Award Recipient: VladimirYurkov
  • NSERC
    • Principle Award Recipient: VladimirYurkov
© 2023 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005980
2023-07-21
2024-05-02
Loading full text...

Full text loading...

References

  1. Maltman C, Piercey-Normore MD, Yurkov V. Tellurite-, tellurate-, and selenite-based anaerobic respiration by strain CM-3 isolated from gold mine tailings. Extremophiles 2015; 19:1013–1019 [View Article] [PubMed]
     [Google Scholar]
  2. Maltman C, Walter G, Yurkov V. A diverse community of metal(loid) oxide respiring bacteria is associated with tube worms in the vicinity of the Juan de Fuca Ridge black smoker field. PLoS One 2016; 11:e0149812 [View Article] [PubMed]
     [Google Scholar]
  3. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 1981; 213:340–342 [View Article] [PubMed]
     [Google Scholar]
  4. Girguis PR, Lee RW, Desaulniers N, Childress JJ, Pospesel M et al. Fate of nitrate acquired by the tubeworm Riftia pachyptila. Appl Environ Microbiol 2000; 66:2783–2790 [View Article] [PubMed]
     [Google Scholar]
  5. Ziemke F, Höfle MG, Lalucat J, Rosselló-Mora R. Reclassification of Shewanella putrefaciens Owen’s genomic group II as Shewanella baltica sp. nov. Int J Syst Bacteriol 1998; 48:179–186 [View Article] [PubMed]
     [Google Scholar]
  6. Myers JM, Antholine WE, Myers CR. Vanadium(V) reduction by Shewanella oneidensis MR-1 requires menaquinone and cytochromes from the cytoplasmic and outer membranes. Appl Environ Microbiol 2004; 70:1405–1412 [View Article] [PubMed]
     [Google Scholar]
  7. Csotonyi JT, Stackebrandt E, Yurkov V. Anaerobic respiration on tellurate and other metalloids in bacteria from hydrothermal vent fields in the eastern Pacific Ocean. Appl Environ Microbiol 2006; 72:4950–4956 [View Article] [PubMed]
     [Google Scholar]
  8. Carpentier W, De Smet L, Van Beeumen J, Brigé A. Respiration and growth of Shewanella oneidensis MR-1 using vanadate as the sole electron acceptor. J Bacteriol 2005; 187:3293–3301 [View Article] [PubMed]
     [Google Scholar]
  9. Klonowska A, Heulin T, Vermeglio A. Selenite and Tellurite Reduction by Shewanella oneidensis. Appl Environ Microbiol 2005; 71:5607–5609 [View Article] [PubMed]
     [Google Scholar]
  10. Valdivia-González MA, Díaz-Vásquez WA, Ruiz-León D, Becerra AA, Aguayo DR et al. A comparative analysis of tellurite detoxification by members of the genus Shewanella. Arch Microbiol 2018; 200:267–273 [View Article] [PubMed]
     [Google Scholar]
  11. Maltman C, Yurkov V. Extreme environments and high-level bacterial tellurite resistance. Microorganisms 2019; 7:12 [View Article] [PubMed]
     [Google Scholar]
  12. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME et al. Towards environmental systems biology of Shewanella. Nat Rev Microbiol 2008; 6:592–603 [View Article] [PubMed]
     [Google Scholar]
  13. Yurkov VV, Van Gemerden H. Abundance and salt tolerance of obligately aerobic, phototrophic bacteria in a marine microbial mat. Neth J Sea Res 1993; 31:57–62 [View Article]
     [Google Scholar]
  14. Jordan EO, Caldwell ME, Reiter D. Bacterial Motility. J Bacteriol 1934; 27:165–174 [View Article] [PubMed]
     [Google Scholar]
  15. Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966; 45:493–496 [PubMed]
     [Google Scholar]
  16. Yurkov V, Stackebrandt E, Holmes A, Fuerst JA, Hugenholtz P et al. Phylogenetic positions of novel aerobic, bacteriochlorophyll a-containing bacteria and description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. Int J Syst Bacteriol 1994; 44:427–434 [View Article] [PubMed]
     [Google Scholar]
  17. Ji-Young K, Han-Su Y, Dong-Heon L, So-Hyun P, Young-Ju K et al. Shewanella algicola sp. nov., a marine bacterium isolated from brown algae. Int J Syst Evol Microbiol 2016; 66:2218–2224 [View Article] [PubMed]
     [Google Scholar]
  18. Kämpfer P, Buczolits S, Albrecht A, Busse H-J, Stackebrandt E. Towards a standardized format for the description of a novel species (of an established genus): Ochrobactrum gallinifaecis sp. nov. Int J Syst Evol Microbiol 2003; 53:893–896 [View Article] [PubMed]
     [Google Scholar]
  19. Folch J, Lees M, Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226:497–509 [PubMed]
     [Google Scholar]
  20. Nguyen TM, Kim J. A rapid and simple method for identifying bacterial polar lipid components in wet biomass. J Microbiol 2017; 55:635–639 [View Article] [PubMed]
     [Google Scholar]
  21. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 1977; 100:221–230 [View Article] [PubMed]
     [Google Scholar]
  22. Chen WP, Kuo TT. A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic Acids Res 1993; 21:2260 [View Article] [PubMed]
     [Google Scholar]
  23. Tamura K, Stecher G, Kumar S, Battistuzzi FU. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article]
     [Google Scholar]
  24. Jain M, Olsen HE, Paten B, Akeson M. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol 2016; 17:256 [View Article] [PubMed]
     [Google Scholar]
  25. Wick RR, Judd LM, Holt KE. Performance of neural network basecalling tools for Oxford Nanopore sequencing. Genome Biol 2019; 20:129 [View Article] [PubMed]
     [Google Scholar]
  26. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
     [Google Scholar]
  27. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2014; 25:1043–1055 [View Article]
     [Google Scholar]
  28. Yoon SH, Ha SM, Lim JM, Kwon SJ, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
     [Google Scholar]
  29. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
     [Google Scholar]
  30. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article] [PubMed]
     [Google Scholar]
  31. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008; 57:758–771 [View Article] [PubMed]
     [Google Scholar]
  32. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  33. Letunic I, Bork P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
     [Google Scholar]
  34. Goffredi SK, Childress JJ, Lallier FH, Desaulniers NT. The ionic composition of the hydrothermal vent tube worm Riftia pachyptila: evidence for the elimination of SO2-4SO and H+ and for a Cl-/HCO-3 shift. Physiol Biochem Zool 1999; 72:296–306 [View Article] [PubMed]
     [Google Scholar]
  35. Wang M-Q, Sun L. Shewanella inventionis sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 2016; 66:4947–4953 [View Article] [PubMed]
     [Google Scholar]
  36. Bozal N, Montes M, Tudela E, Jimenez F, Guinea J. Shewanella frigidimarina and Shewanella livingstonensis sp. nov. isolated from Antarctic costal areas. Int J Syst Evol Microbiol 2002; 52:195–205 [View Article] [PubMed]
     [Google Scholar]
  37. Toffin L, Bidault A, Pignet P, Tindall BJ, Slobodkin A et al. Shewanella profunda sp. nov., isolated from deep marine sediment of the Nankai Trough. Int J Syst Evol Microbiol 2004; 54:1943–1949 [View Article] [PubMed]
     [Google Scholar]
  38. Bozal N, Montes MJ, Miñana-Galbis D, Manresa A, Mercadé E. Shewanella vesiculosa sp. nov., a psychrotolerant bacterium isolated from an Antarctic coastal area. Int J Syst Evol Microbiol 2009; 59:336–340 [View Article] [PubMed]
     [Google Scholar]
  39. Ho-Won C, Seong R, Kyoung-Ho K, Young-Do N, Che J et al. Shewanella basaltis sp. nov., a marine bacterium isolated from black sand. Int J Syst Evol Microbiol 2008; 58:1907–1910 [View Article] [PubMed]
     [Google Scholar]
  40. Yun B-R, Park S, Kim M-K, Park J, Kim SB. Shewanella saliphila sp. nov., Shewanella ulleungensis sp. nov. and Shewanella litoralis sp. nov., isolated from coastal seawater. Int J Syst Evol Microbiol 2018; 68:2960–2966 [View Article] [PubMed]
     [Google Scholar]
  41. Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J et al. Shewanella. In Bergey’s Manual of Systematics of Archaea and Bacteria New York, NY: John Wiley & Sons; 2015 pp 1–22 [View Article]
     [Google Scholar]
  42. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
     [Google Scholar]
  43. Yurkov V, Jappe J, Vermeglio A. Tellurite resistance and reduction by obligately aerobic photosynthetic bacteria. Appl Environ Microbiol 1996; 62:4195–4198 [View Article] [PubMed]
     [Google Scholar]
  44. Monfort O, Petrisková P. Binary and ternary vanadium oxides: general overview, physical properties, and photochemical processes for environmental applications. Processes 2021; 9:214 [View Article]
     [Google Scholar]
  45. Csotonyi JT, Maltman C, Swiderski J, Stackebrandt E, Yurkov V. Extremely “vanadiphilic” multiply metal-resistant and halophilic aerobic anoxygenic phototrophs, strains EG13 and EG8, from hypersaline springs in Canada. Extremophiles 2015; 19:127–134 [View Article] [PubMed]
     [Google Scholar]
  46. Kuzyk SB, Wiens K, Ma X, Yurkov V. Association of aerobic anoxygenic phototrophs and zebra mussels, Dreissena polymorpha, within the littoral zone of Lake Winnipeg. J Great Lakes Res 2020; 47:567–582 [View Article]
     [Google Scholar]
  47. Xu M, Guo J, Cen Y, Zhong X, Cao W et al. Shewanella decolorationis sp. nov., a dye-decolorizing bacterium isolated from activated sludge of a waste-water treatment plant. Int J Syst Evol Microbiol 2005; 55:363–368 [View Article] [PubMed]
     [Google Scholar]
  48. Satomi M, Vogel BF, Gram L, Venkateswaran K. Shewanella hafniensis sp. nov. and Shewanella morhuae sp. nov., isolated from marine fish of the Baltic Sea. Int J Syst Evol Microbiol 2006; 56:243–249 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005980
Loading
Shewanella metallivivens sp. nov., a deep-sea hydrothermal vent tube worm endobiont capable of dissimilatory anaerobic metalloid oxyanion reduction
Int J Syst Evol Microbiol 73, 005980 (2023); https://doi.org/10.1099/ijsem.0.005980
/content/journal/ijsem/10.1099/ijsem.0.005980
/content/journal/ijsem/10.1099/ijsem.0.005980
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Supplementary material 3

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error