Geothermobacter hydrogeniphilus sp. nov., a mesophilic, iron(III)-reducing bacterium from seafloor/subseafloor environments in the Pacific Ocean, and emended description of the genus Geothermobacter

Ileana Pérez-Rodríguez; Jessica K. Choi; Karla Abuyen; Madeline Tyler; Cynthia Ronkowski; Eric Romero; Anthony Trujillo; Jason Tremblay; Isabella Viney; Pratixaben Savalia; Jan P. Amend

doi:10.1099/ijsem.0.004739

Volume 71, Issue 4

Research Article

Free

Geothermobacter hydrogeniphilus sp. nov., a mesophilic, iron(III)-reducing bacterium from seafloor/subseafloor environments in the Pacific Ocean, and emended description of the genus Geothermobacter

Ileana Pérez-Rodríguez^1,2,3,†, Jessica K. Choi^1,†, Karla Abuyen^2,4,5,†, Madeline Tyler^4,‡, Cynthia Ronkowski⁴, Eric Romero^4,§, Anthony Trujillo⁴, Jason Tremblay⁴, Isabella Viney^1,#, Pratixaben Savalia² and Jan P. Amend^2,5
View Affiliations Hide Affiliations

Affiliations: ¹ Department of Earth and Environmental Science, University of Pennsylvania, Philadelphia, PA 19104, USA ² Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089, USA ³ Geophysical Laboratory, Carnegie Institution of Washington, Washington, DC 20015, USA ⁴ Community College Cultivation Cohort, University of Southern California, Los Angeles, CA 90089, USA ⁵ Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089, USA ^‡ Present address: College of Pharmacy, Oregon State University, Corvallis, OR 97330, USA ^§ Present address: Department of Nuclear Engineering, University of California, Berkeley, CA 94720, USA ^# Present address: Department of Microbiology, University of Arizona, Tucson, AZ 85721, USA
*Correspondence: Ileana Pérez-Rodríguez, [email protected]

† These authors contributed equally to this work
Published: 20 April 2021 https://doi.org/10.1099/ijsem.0.004739

Abstract

A novel mesophilic, anaerobic, mixotrophic bacterium, with designated strains EPR-MT and HR-1, was isolated from a semi-extinct hydrothermal vent at the East Pacific Rise and from an Fe-mat at Lō'ihi Seamount, respectively. The cells were Gram-negative, pleomorphic rods of about 2.0 µm in length and 0.5 µm in width. Strain EPR-MT grew between 25 and 45 °C (optimum, 37.5–40 °C), 10 and 50 g l−1 NaCl (optimum, 15–20 g l−1) and pH 5.5 and 8.6 (optimum, pH 6.4). Strain HR-1 grew between 20 and 45 °C (optimum, 37.5–40 °C), 10 and 50 g l−1 NaCl (optimum, 15–25 g l−1) and pH 5.5 and 8.6 (optimum, pH 6.4). Shortest generation times with H2 as the primary electron donor, CO2 as the carbon source and ferric citrate as terminal electron acceptor were 6.7 and 5.5 h for EPR-MT and HR-1, respectively. Fe(OH)3, MnO2, AsO4 3-, SO4 2-, SeO4 2-, S2O3 2-, S0 and NO3 - were also used as terminal electron acceptors. Acetate, yeast extract, formate, lactate, tryptone and Casamino acids also served as both electron donors and carbon sources. G+C content of the genomic DNA was 59.4 mol% for strain EPR-MT and 59.2 mol% for strain HR-1. Phylogenetic and phylogenomic analyses indicated that both strains were closely related to each other and to Geothermobacter ehrlichii , within the class δ- Proteobacteria (now within the class Desulfuromonadia ). Based on phylogenetic and phylogenomic analyses in addition to physiological and biochemical characteristics, both strains were found to represent a novel species within the genus Geothermobacter , for which the name Geothermobacter hydrogeniphilus sp. nov. is proposed. Geothermobacter hydrogeniphilus is represented by type strain EPR-MT (=JCM 32109T=KCTC 15831T=ATCC TSD-173T) and strain HR-1 (=JCM 32110=KCTC 15832).

Received: 22/07/2020
Accepted: 14/02/2021
Published Online: 20/04/2021

Keyword(s): deep-sea hydrothermal vents , Deltaproteobacteria , Desulfuromonadia , dissimilatory Fe(III) reduction , hydrogen oxidation and seamount

Funding

This study was supported by the:

NSF Science and Technology Center (C-DEBI) (Award OCE-1431598)
- Principle Award Recipient: JanAmend
Center for Dark Energy Biosphere Investigations (Award OCE-1460892)
- Principle Award Recipient: JanAmend
University of Pennsylvania (Award University of Pennsylvania (Penn) Start-up Funds and Elliman Faculty Fellowship)
- Principle Award Recipient: IleanaM. Pérez-Rodríguez
Center for Dark Energy Biosphere Investigations (Award Postdoctoral Fellowship)
- Principle Award Recipient: IleanaM. Pérez-Rodríguez

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004739

2021-04-20

2024-04-24

Full text loading...

/deliver/fulltext/ijsem/71/4/ijsem004739.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004739&mimeType=html&fmt=ahah

References

Waite DW, Chuvochina M, Pelikan C, Parks DH, Yilmaz P et al. Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol 2020; 70:5972–6016 [View Article][PubMed]
[Google Scholar]
Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S et al. NCBI taxonomy: a comprehensive update on curation, resources and tools. Database 2020; 2020: 01 01 2020 [View Article][PubMed]
[Google Scholar]
Röling WFM. The family Geobacteraceae . In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes Berlin, Heidelberg: Springer; 2014 [View Article]
[Google Scholar]
Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJ et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 1993; 159:336–344 [View Article][PubMed]
[Google Scholar]
Kashefi K, Holmes DE, Baross JA, Lovley DR. Thermophily in the Geobacteraceae: Geothermobacter ehrlichii gen. nov., sp. nov., a novel thermophilic member of the Geobacteraceae from the "Bag City" hydrothermal vent. Appl Environ Microbiol 2003; 69:2985–2993 [View Article][PubMed]
[Google Scholar]
Holmes DE, Nicoll JS, Bond DR, Lovley DR. Potential role of a novel psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by a marine sediment fuel cell. Appl Environ Microbiol 2004; 70:6023–6030 [View Article][PubMed]
[Google Scholar]
Zavarzina DG, Kolganova TV, Bulygina ES, Kostrikina NA, Turova TP et al. Geoalkalibacter ferrihydriticus gen. nov., sp. nov., the first alkaliphilic representative of the family Geobacteraceae, isolated from a soda lake]. Mikrobiologiia 2006; 75:673–682 [View Article][PubMed]
[Google Scholar]
Xu Z, Masuda Y, Itoh H, Ushijima N, Shiratori Y et al. Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., Four Ferric-Reducing Bacteria Isolated From Paddy Soil, and Reclassification of Three Species of the Genus Geobacter as Members of the Genus Geomonas gen. nov. Front Microbiol 2019; 10:2201 [View Article][PubMed]
[Google Scholar]
Lovley DR, Phillips EJ. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 1988; 54:1472–1480 [View Article][PubMed]
[Google Scholar]
Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF et al. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 1994; 60:3752–3759 [View Article][PubMed]
[Google Scholar]
Nevin KP, Holmes DE, Woodard TL, Hinlein ES, Ostendorf DW et al. Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates. Int J Syst Evol Microbiol 2005; 55:1667–1674 [View Article][PubMed]
[Google Scholar]
Coates JD, Bhupathiraju VK, Achenbach LA, Mclnerney MJ, Lovley DR. Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 2001; 51:581–588 [View Article][PubMed]
[Google Scholar]
Straub KL, Buchholz-Cleven BE. Geobacter bremensis sp. nov. and Geobacter pelophilus sp. nov., two dissimilatory ferric-iron-reducing bacteria. Int J Syst Evol Microbiol 2001; 51:1805–1808 [View Article][PubMed]
[Google Scholar]
Sung Y, Fletcher KE, Ritalahti KM, Apkarian RP, Ramos-Hernández N et al. Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl Environ Microbiol 2006; 72:2775–2782 [View Article][PubMed]
[Google Scholar]
Nevin KP, Holmes DE, Woodard TL, Covalla SF, Lovley DR. Reclassification of Trichlorobacter thiogenes as Geobacter thiogenes comb. nov. Int J Syst Evol Microbiol 2007; 57:463–466 [View Article][PubMed]
[Google Scholar]
Shelobolina ES, Nevin KP, Blakeney-Hayward JD, Johnsen CV, Plaia TW et al. Geobacter pickeringii sp. nov., Geobacter argillaceus sp. nov. and Pelosinus fermentans gen. nov., sp. nov., isolated from subsurface kaolin lenses. Int J Syst Evol Microbiol 2007; 57:126–135 [View Article][PubMed]
[Google Scholar]
Shelobolina ES, Vrionis HA, Findlay RH, Lovley DR. Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioremediation. Int J Syst Evol Microbiol 2008; 58:1075–1078 [View Article][PubMed]
[Google Scholar]
Kunapuli U, Jahn MK, Lueders T, Geyer R, Heipieper HJ et al. Desulfitobacterium aromaticivorans sp. nov. and Geobacter toluenoxydans sp. nov., iron-reducing bacteria capable of anaerobic degradation of monoaromatic hydrocarbons. Int J Syst Evol Microbiol 2010; 60:686–695 [View Article][PubMed]
[Google Scholar]
Prakash O, Gihring TM, Dalton DD, Chin K-J, Green SJ et al. Geobacter daltonii sp. nov., an Fe(III)- and uranium(VI)-reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination. Int J Syst Evol Microbiol 2010; 60:546–553 [View Article][PubMed]
[Google Scholar]
Viulu S, Nakamura K, Okada Y, Saitou S, Takamizawa K. Geobacter luticola sp. nov., an Fe(III)-reducing bacterium isolated from lotus field mud. Int J Syst Evol Microbiol 2013; 63:442–448 [View Article][PubMed]
[Google Scholar]
Sun D, Wang A, Cheng S, Yates M, Logan BE. Geobacter anodireducens sp. nov., an exoelectrogenic microbe in bioelectrochemical systems. Int J Syst Evol Microbiol 2014; 64:3485–3491 [View Article][PubMed]
[Google Scholar]
Zhou S, Yang G, Lu Q, Wu M. Geobacter soli sp. nov., a dissimilatory Fe(III)-reducing bacterium isolated from forest soil. Int J Syst Evol Microbiol 2014; 64:3786–3791 [View Article][PubMed]
[Google Scholar]
Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM et al. Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv Microb Physiol 2011; 59:1–99 [View Article][PubMed]
[Google Scholar]
Slobodkina GB, Kolganova TV, Querellou J, Bonch-Osmolovskaya EA, Slobodkin AI. Geoglobus acetivorans sp. nov., an iron(III)-reducing archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 2009; 59:2880–2883 [View Article][PubMed]
[Google Scholar]
Sleat R, Mah RA, Robinson R. Isolation and characterization of an anaerobic, cellulolytic bacterium, Clostridium cellulovorans sp. nov. Appl Environ Microbiol 1984; 48:88–93 [View Article][PubMed]
[Google Scholar]
Tschech A, Schink B. Fermentative degradation of resorcinol and resorcylic acids. Arch Microbiol 1985; 143:52–59 [View Article]
[Google Scholar]
Wolin EA, Wolin MJ, Wolfe RS. Formation of methane by bacterial extracts. J Biol Chem 1963; 238:2882–2886 [View Article][PubMed]
[Google Scholar]
Pérez-Rodríguez I, Rawls M, Coykendall DK, Foustoukos DI. Deferrisoma palaeochoriense sp. nov., a thermophilic, iron(III)-reducing bacterium from a shallow-water hydrothermal vent in the Mediterranean Sea. Int J Syst Evol Microbiol 2016; 66:830–836 [View Article][PubMed]
[Google Scholar]
Tully B, Savalia P, Abuyen K, Baughan C, Romero E et al. Genome sequence of Geothermobacter sp. strain EPR-M, a deep-sea hydrothermal vent iron reducer. Genome Announc 2017; 5:e00424–17 [View Article][PubMed]
[Google Scholar]
Emerson D. Potential for Iron-reduction and Iron-cycling in iron Oxyhydroxide-rich microbial mats at Loihi Seamount. Geomicrobiol J 2009; 26:639–647 [View Article]
[Google Scholar]
McBeth JM, Little BJ, Ray RI, Farrar KM, Emerson D. Neutrophilic iron-oxidizing "zetaproteobacteria" and mild steel corrosion in nearshore marine environments. Appl Environ Microbiol 2011; 77:1405–1412 [View Article][PubMed]
[Google Scholar]
Stookey LL. Ferrozine---a new spectrophotometric reagent for iron. Anal Chem 1970; 42:779–781 [View Article]
[Google Scholar]
Smith H, Abuyen K, Tremblay J, Savalia P, Pérez-Rodríguez I et al. Genome sequence of Geothermobacter sp. strain HR-1, an Iron reducer from the Lō'ihi Seamount, Hawai'i. Genome Announc 2018; 6:e00339–18 [View Article][PubMed]
[Google Scholar]
Orcutt B, Wheat CG, Edwards KJ. Subseafloor Ocean crust microbial Observatories: development of FLOCS (flow-through Osmo colonization system) and evaluation of Borehole construction materials. Geomicrobiol J 2010; 27:143–157 [View Article]
[Google Scholar]
Forget NL, Murdock SA, Juniper SK. Bacterial diversity in Fe-rich hydrothermal sediments at two South Tonga Arc submarine volcanoes. Geobiology 2010; 8:417–432 [View Article][PubMed]
[Google Scholar]
Darjany LE, Whitcraft CR, Dillon JG. Lignocellulose-responsive bacteria in a southern California salt marsh identified by stable isotope probing. Front Microbiol 2014; 5:263 [View Article][PubMed]
[Google Scholar]
Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article][PubMed]
[Google Scholar]
Yoon S-H, Ha S-M, Lim J, Kwon S, 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]
Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article][PubMed]
[Google Scholar]
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
[Google Scholar]
Miller LT. A single derivatization method for bacterial fatty acid methyl esters including hydroxy acids. J Clin Microbiol 1982; 16:584–586
[Google Scholar]
Kuykendall LD, Roy MA, O'Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum . Int J Syst Bacteriol 1988; 38:358–361 [View Article]
[Google Scholar]
Euzéby JP. Validation List no. 102. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2005; 55:547–549
[Google Scholar]

http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004739

Geothermobacter hydrogeniphilus sp. nov., a mesophilic, iron(III)-reducing bacterium from seafloor/subseafloor environments in the Pacific Ocean, and emended description of the genus Geothermobacter

Int J Syst Evol Microbiol 71, 004739 (2021); https://doi.org/10.1099/ijsem.0.004739

/content/journal/ijsem/10.1099/ijsem.0.004739

Data & Media loading...

Supplements

Volume 71, Issue 4

Research Article

Free

Geothermobacter hydrogeniphilus sp. nov., a mesophilic, iron(III)-reducing bacterium from seafloor/subseafloor environments in the Pacific Ocean, and emended description of the genus Geothermobacter

Abstract

Funding

Supplementary material 1

Most read this month

Most cited Most Cited RSS feed

Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies

DNA–DNA hybridization values and their relationship to whole-genome sequence similarities

A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae

OrthoANI: An improved algorithm and software for calculating average nucleotide identity

Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes

List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ

Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes

Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium

Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology

Valid publication of the names of forty-two phyla of prokaryotes