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Microbial community of recently discovered Auka vent field sheds light on vent biogeography and evolutionary history of thermophily

Speth, Daan R. and Yu, Feiqiao B. and Connon, Stephanie A. and Lim, Sujung and Magyar, John S. and Peña, Manet E. and Quake, Stephen R. and Orphan, Victoria J. (2021) Microbial community of recently discovered Auka vent field sheds light on vent biogeography and evolutionary history of thermophily. . (Unpublished)

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Hydrothermal vents have been key to our understanding of the limits of life, and the metabolic and phylogenetic diversity of thermophilic organisms. Here we used environmental metagenomics combined with analysis of physico-chemical data and 16S rRNA amplicons to characterize the diversity, temperature optima, and biogeographic distribution of sediment-hosted microorganisms at the recently discovered Auka vents in the Gulf of California, the deepest known hydrothermal vent field in the Pacific Ocean. We recovered 325 metagenome assembled genomes (MAGs) representing 54 phyla, over 1/3 of the currently known phylum diversity, showing the microbial community in Auka hydrothermal sediments is highly diverse. Large scale 16S rRNA amplicon screening of 227 sediment samples across the vent field indicates that the MAGs are largely representative of the microbial community. Metabolic reconstruction of a vent-specific, deeply branching clade within the Desulfobacterota (Tharpobacteria) suggests these organisms metabolize sulfur using novel octaheme cytochrome-c proteins related to hydroxylamine oxidoreductase. Community-wide comparison of the average nucleotide identity of the Auka MAGs with MAGs from the Guaymas Basin vent field, found 400 km to the Northwest, revealed a remarkable 20% species-level overlap between vent sites, suggestive of long-distance species transfer and sediment colonization. An adapted version of a recently developed model for predicting optimal growth temperature to the Auka and Guaymas MAGs indicates several of these uncultured microorganisms could grow at temperatures exceeding the currently known upper limit of life. Extending this analysis to reference data shows that thermophily is a trait that has evolved frequently among Bacteria and Archaea. Combined, our results show that Auka vent field offers new perspectives on our understanding of hydrothermal vent microbiology.

Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription Paper ItemData
Speth, Daan R.0000-0002-2361-5935
Yu, Feiqiao B.0000-0003-3416-3046
Lim, Sujung0000-0001-6040-729X
Magyar, John S.0000-0002-3586-8286
Peña, Manet E.0000-0002-5835-0455
Quake, Stephen R.0000-0002-1613-0809
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license. This version posted August 2, 2021. We thank the pilots, crew, and participants on the cruises to the southern Gulf of California: R/V Western Flyer operated by the Monterey Bay Aquarium Research Institute (MBARI), E/V Nautlius operated by the Ocean Exploration Trust, with cruise NA091 supported by the Dalio Foundation and Woods Hole Oceanographic Institute, and R/V Falkor operated by the Schmidt Ocean Institute. We appreciate the support and opportunity to sail with chief scientists Scott Wankel and Anna Michel on NA091. We also thank David W. Caress and Jennifer B. Paduan (MBARI) for providing the high resolution version of the bathymetric map in Figure 1, David Sauer for recalculating the optimal growth temperature prediction model to be appropriate for metagenomics, and Haley Sapers for providing a framework for the 16S rRNA gene amplicon processing. This research used samples provided by the Ocean Exploration Trust’s Nautilus Exploration Program, cruise NA091. This work was supported by the Center for Dark Energy Biosphere investigations (C-DEBI), Canadian Institute for Advanced Science (CIFAR), the US Department of Energy, Office of Science, Office of Biological and Environmental Research under award number DE-SC0016469 to Victoria J. Orphan. Daan R. Speth was supported by the Netherlands Organisation for Scientific Research, Rubicon award 019.153LW.039. Feiqiao B. Yu and Stephen R. Quake were supported by the John Templeton Foundation grant 51250 and the Chan Zuckerberg Biohub. Victoria J. Orphan is a CIFAR fellow in the Earth 4D program. Sample collection permits were granted by la Dirección General de Ordenamiento Pesquero y Acuícola, Comisión Nacional de Acuacultura y Pesca (CONAPESCA: Permiso de Pesca de Fomento No. PPFE/DGOPA-200/18) and l a Dirección G eneral de G eografía y Medio A mbiente, Instituto Nacional de Estadística y Geografía (INEGI: Autorización EG0122018), with t he associated Diplomatic Note number 18-2083 (CTC/07345/18) f rom l a Secretaría d e R elaciones Exteriores - Agencia Mexicana de Cooperación I nternacional para el Desarrollo / Dirección General de Cooperación Técnica y Científica. Sample collection permit for cruise NA091 was obtained by the Ocean Exploration T rust under permit number EG0072017. Data availability: Raw metagenome reads, assembled metagenome bins, and 16S rRNA gene amplicon sequencing data are available in GenBank under BioProject accession number PRJNA713414. The authors have declared no competing interest.
Funding AgencyGrant Number
Center for Dark Energy Biosphere investigations (C-DEBI)UNSPECIFIED
Canadian Institute for Advanced Research (CIFAR)UNSPECIFIED
Department of Energy (DOE)DE-SC0016469
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)019.153LW.039
John Templeton Foundation51250
Chan Zuckerberg InitiativeUNSPECIFIED
Record Number:CaltechAUTHORS:20210804-220359405
Persistent URL:
Official Citation:Microbial community of recently discovered Auka vent field sheds light on vent biogeography and evolutionary history of thermophily. Daan R. Speth, Feiqiao B. Yu, Stephanie A. Connon, Sujung Lim, John S. Magyar, Manet E. Peña, Stephen R. Quake, Victoria J. Orphan. bioRxiv 2021.08.02.454472; doi:
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110149
Deposited By: Tony Diaz
Deposited On:04 Aug 2021 22:20
Last Modified:16 Nov 2021 19:39

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