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Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov.

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Abstract

A novel iron-oxidizing chemolithoautotrophic bacterium, strain ET2T, was isolated from a deep-sea sediment in a hydrothermal field of the Bayonnaise knoll of the Izu-Ogasawara arc. Cells were bean-shaped, curved short rods. Growth was observed at a temperature range of 15–30 °C (optimum 25 °C, doubling time 24 h) and a pH range of 5.8–7.0 (optimum pH 6.4) in the presence of NaCl at a range of 1.0–4.0 % (optimum 2.75 %). The isolate was a microaerophilic, strict chemolithoautotroph capable of growing using ferrous iron and molecular oxygen (O2) as the sole electron donor and acceptor, respectively; carbon dioxide as the sole carbon source; and either ammonium or nitrate as the sole nitrogen source. Phylogenetic analysis based on the 16S rRNA gene sequence indicated that the new isolate was related to the only previously isolated Mariprofundus species, M. ferrooxydans. Although relatively high 16S rRNA gene similarity (95 %) was found between the new isolate and M. ferrooxydans, the isolate was distinct in terms of cellular fatty acid composition, genomic DNA G+C content and cell morphology. Furthermore, genomic comparison between ET2T and M. ferrooxydans PV-1 indicated that the genomic dissimilarity of these strains met the standard for species-level differentiation. On the basis of its physiological and molecular characteristics, strain ET2T (= KCTC 15556T = JCM 30585 T) represents a novel species of Mariprofundus, for which the name Mariprofundus micogutta is proposed. We also propose the subordinate taxa Mariprofundales ord. nov. and Zetaproteobacteria classis nov. in the phylum Proteobacteria.

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References

  • Abraham WR, Rhode M (2014) The family Hyphomonadaceae. In: Rosenberg E et al (eds) The Prokaryotes. Springer, New York, pp 283–299

    Chapter  Google Scholar 

  • Abraham WR, Strömpl C, Meyer H, Lindholst S, Moore ER, Christ R, Vancanneyt M, Tindall BJ, Bennasar A, Smit J, Tesar M (1999) Phylogeny and polyphasic taxonomy of Caulobacter species. Proposal of Maricaulis gen. nov. with Maricaulis maris (Poindexter) comb. nov. as the type species, and emended description of the genera Brevundirnonas and Caulobacter. Int J Syst Bacteriol 49(3):1053–1073

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its application to single-cell sequencing. J Comput Biol 19:455–477. doi:10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baquiran JP, Ramírez GA, Haddad AG, Toner BM, Hulme S, Wheat CG, Edwards KJ, Orcutt BN (2016) Temperature and redox effect on mineral colonization in Juan de Fuca Ridge flank subsurface crustal fluids. Front Microbiol 7:396. doi:10.3389/fmicb.2016.00396 eCollection 2016

    Article  PubMed  PubMed Central  Google Scholar 

  • Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF (1998) Genbank. Nucleic Acids Res 26:1–7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan CS, Fakra SC, Emerson D, Fleming EJ, Edwards KJ (2011) Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. ISME J 5:717–727

    Article  CAS  PubMed  Google Scholar 

  • Davis RE, Moyer C (2008) Extreme spatial and temporal variability of hydrothermal microbial mat communities along the Mariana Island Arc and southern Mariana back-arc system. J Geophys Res 113:B08S15. doi:10.1029/2007JB005413

    Google Scholar 

  • Emerson D, Floyd MM (2005) Enrichment and isolation of iron-oxidizing bacteria at neutral pH. Methods Enzymol 397:112–123

    Article  CAS  PubMed  Google Scholar 

  • Emerson D, Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792

    CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson D, Moyer C (2002) Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl Environ Microbiol 68:3085–3093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, Moyer CL (2007) A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS One 2:e667

    Article  PubMed  PubMed Central  Google Scholar 

  • Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583

    Article  CAS  PubMed  Google Scholar 

  • Emerson D, Field EK, Chertkov O, Davenport KW, Goodwin L, Munk C, Nolan M, Woyke T (2013) Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front Microbiol 4:254. doi:10.3389/fmicb.2013.00254 eCollection2013

    Article  PubMed  PubMed Central  Google Scholar 

  • Forget NL, Murdock SA, Juniper SK (2010) Bacterial diversity in Fe-rich hydrothermal sediments at two South Tonga Arc submarine volcanoes. Geobiology 8:417–432. doi:10.1111/j.1472-4669.2010.00247.x

    Article  CAS  PubMed  Google Scholar 

  • Gillis M, Vandamme P, De Vos P, Swings J, Kersters K (2001) Polyphasic taxonomy. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology (The archaea and the deeply branching and phototrophic bacteria), vol 1, 2nd edn. Springer, New York, pp 43–48

    Google Scholar 

  • Hallbeck L, Pedersen K (1990) Culture parameters regulating stalk formation and growth rate of Gallionella ferruginea. J Gen Microbiol 136:1675–1680

    Article  Google Scholar 

  • Hallbeck L, Pedersen K (1991) Autotrophic and mixotrophic growth of Gallionella ferruginea. J Gen Microbiol 137:2657–2661

    Article  CAS  Google Scholar 

  • Hallbeck L, Ståhl F, Pedersen K (1993) Phylogeny and phenotypic characterization of the stalk-forming and iron-oxidizing bacterium Gallionella ferruginea. J Gen Microbiol 139:1531–1535

    Article  CAS  PubMed  Google Scholar 

  • Hanert HH (2006) The genus Gallionella. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stacke-Brandt E (eds) The Prokaryotes, vol 7. Springer, New York, pp 990–995

    Chapter  Google Scholar 

  • Hodges TW, Olson JB (2009) Molecular comparison of bacterial communities within iron-containing flocculent mats associated with submarine volcanoes along the Kermadec Arc. Appl Environ Microbiol 75:1650–1657

    Article  CAS  PubMed  Google Scholar 

  • Kato S, Kobayashi C, Kakegawa T, Yamagishi A (2009) Microbial communities in iron-silica-rich microbial mats at deepsea hydrothermal fields of the Southern Mariana Trough. Environ Microbiol 11:2094–2111

    Article  CAS  PubMed  Google Scholar 

  • Kato S, Chan C, Itoh T, Ohkuma M (2013) Functional gene analysis of freshwater iron-rich flocs at circumneutral pH and isolation of a stalk-forming microaerophilic iron-oxidizing bacterium. Appl Environ Microbiol 79:5283–5290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennedy CB, Scott SD, Ferris FG (2003) Ultra structure and potential sub-seafloor evidence of bacteriogenic iron oxides from Axial Volcano, Juan de Fuca Ridge, north-east Pacific Ocean. FEMS Microbiol Ecol 43:247–254. doi:10.1111/j.1574-6941.2003.tb01064.x

    Article  CAS  PubMed  Google Scholar 

  • Komagata K, Suzuki K (1987) Lipid and cell-wall analysis in bacterial systematics. Method Microbiol 19:161–207

    Article  CAS  Google Scholar 

  • Kostka JE, Luther GW III (1994) Partitioning and speciation of solid phase iron in saltmarsh sediments. Geochim Cosmochim Acta 58:1701–1710

    Article  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Dworkin M, Falkow S, Stackebrandt E, Goodfellow M, Chichester (eds) Nucleic acid techniques in bacterial systematics. Wiley, Hoboken, pp 115–175

    Google Scholar 

  • Lee I, Kim YO, Park SC, Chun J (2015) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.000760

    Google Scholar 

  • Makita H, Nakagawa S, Miyazaki M, Nakamura K, Inagaki F, Takai K (2012) Thiofractor thiocaminus gen. nov., sp. nov., a novel hydrogen-oxidizing, sulfur-reducing epsilonproteobacterium isolated from a deep-sea hydrothermal vent chimney in the Nikko Seamount field of the northern Mariana Arc. Arch Microbiol 194(9):785–794. doi:10.1007/s00203-012-0814-1

    Article  CAS  PubMed  Google Scholar 

  • Makita H, Kikuchi S, Mitsunobu S, Takaki Y, Yamanaka T, Toki T, Noguchi T, Nakamura K, Abe M, Hirai M, Yamamoto M, Uematsu K, Miyazaki J, Nunoura T, Takahashi Y, Takai K (2016) Comparative analysis of microbial communities in iron-dominated flocculent mats in Deep Sea hydrothermal environments. Appl Environ Microbiol. doi:10.1128/AEM.01151-16

    PubMed  Google Scholar 

  • Masuda H, Fryer P, Ishibashi J, Toki T, Shitashima K, Kimura H, Suzuki R, Sato S, Takemoto K, Kato S, Kobayashi C, Kuno M, Noguchi T, Aoki M (2005) Yokosuka YK05-09 Leg2 Cruise report. http://www.godac.jamstec.go.jp/catalog/data/doc_catalog/media/YK05-09_leg2_all.pdf

  • McAllister SM, Davis RE, McBeth JM, Tebo BM, Emerson D, Moyer CL (2011) Biodiversity and emerging biogeography of the neutrophilic iron-oxidizing Zetaproteobacteria. Appl Environ Microbiol 77(15):5445–5457. doi:10.1128/AEM.00533-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McBeth JM, Little BJ, Ray RI, Farrar KM, Emerson D (2011) Neutrophilic iron-oxidizing “Zetaproteobacteria” and mild steel corrosion in nearshore marine environments. Appl Environ Microbiol 77:1405–1412

    Article  CAS  PubMed  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. doi:10.1186/1471-2105-14-60

    Article  PubMed  PubMed Central  Google Scholar 

  • Moreira APB, Meirelles PM, Thompson F (2014) The family Mariprofundaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The  Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria, Springer, pp 403–413. doi:10.1007/978-3-642-39044-9_378

  • Moriya Y, Itoh M, Okuda S, Yoshizawa A, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    Article  PubMed  PubMed Central  Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhou J, Oren A, Zhang YZ (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215

    Article  PubMed  PubMed Central  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069

    Article  CAS  PubMed  Google Scholar 

  • Singer E, Emerson D, Webb EA, Barco RA, Kuenen JG, Nelson WC, Chan CS, Comolli LR, Ferriera S, Johnson J, Heidelberg JF, Edwards KJ (2011) Mariprofundus ferrooxydans PV-1 the first genome of a marine Fe(II) oxidizing Zetaproteobacterium. PLoS One 6(9):e25386. doi:10.1371/journal.pone.0025386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staudigel H, Hart SR, Pile A, Bailey BE, Baker ET, Brooke S, Connelly DP, Haucke L, German CR, Hudson I, Jones D, Koppers AA, Konter J, Lee R, Pietsch TW, Tebo BM, Templeton AS, Zierenberg R, Young CM (2006) Vailulu’u Seamount, Samoa: life and death on an active submarine volcano. Proc Natl Acad Sci USA 103(17):6448–6453. doi:10.1073/pnas.0600830103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sylvan JB, Toner BM, Edwards KJ (2012) Life and death of deep-sea vents: bacterial diversity and ecosystem. Mbio 3(1):e00279. doi:10.1128/mBio.00279-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Veen WL, Mulder EG, Denema MH (1978) The Sphaerotilus-Leptothrix group of bacteria. Microbiol Rev 42:329–356

    PubMed  PubMed Central  Google Scholar 

  • Zillig W, Holz I, Janekovic D, Janekovic D, Klenk HP, Imsel E, Trent J, Wunderl S, Forjaz VH, Coutinho R, Ferreira T (1990) Hyperthermus butylicus, a hyperthermophilic sulfur-reducing archaebacterium that ferments peptides. J Bacteriol 172:3959–3965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank the captain and crew of the R/V Natsushima, the operation team of the ROV Hyper-Dolphin and chief scientist Dr. Motohiro Shimanaga (Kumamoto University) for their valuable help in obtaining deep-sea hydrothermal vent samples during cruise NT14-06. We also thank Mr. Akihiro Tame for his excellent assistance in preparing samples for electron microscopy. We are grateful to Dr. Chong Chen for his help in improving this manuscript. This work was partially supported by JSPS KAKENHI Grant Number JP26820389.

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Correspondence to Hiroko Makita.

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Communicated by Erko Stackebrandt.

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Makita, H., Tanaka, E., Mitsunobu, S. et al. Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov.. Arch Microbiol 199, 335–346 (2017). https://doi.org/10.1007/s00203-016-1307-4

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