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Published July 2022 | Supplemental Material + Published
Journal Article Open

Microbial communities of Auka hydrothermal sediments shed light on vent biogeography and the evolutionary history of thermophily

Abstract

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 physicochemical data and 16S rRNA gene amplicons to characterize the sediment-hosted microorganisms at the recently discovered Auka vents in the Gulf of California. We recovered 325 metagenome assembled genomes (MAGs) representing 54 phyla, over 30% of those currently known, showing the microbial community in Auka hydrothermal sediments is highly diverse. 16S rRNA gene amplicon screening of 224 sediment samples across the vent field indicates that the MAGs retrieved from a single site are representative of the microbial community in the vent field sediments. Metabolic reconstruction of a vent-specific, deeply branching clade within the Desulfobacterota suggests these organisms metabolize sulfur using novel octaheme cytochrome-c proteins related to hydroxylamine oxidoreductase. Community-wide comparison between Auka MAGs and MAGs from Guaymas Basin revealed a remarkable 20% species-level overlap, suggestive of long-distance species transfer over 400 km and subsequent sediment colonization. Optimal growth temperature prediction on the Auka MAGs, and thousands of reference genomes, shows that thermophily is a trait that has evolved frequently. Taken together, our Auka vent field results offer new perspectives on our understanding of hydrothermal vent microbiology.

Additional Information

© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 15 September 2021; Revised 18 January 2022; Accepted 09 February 2022; Published 28 March 2022. 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 Fig. 1, David Sauer for recalculating the optimal growth temperature prediction model to be appropriate for metagenomics, Haley Sapers for providing a framework for the 16S rRNA gene amplicon processing, and Mark Pallen for assistance with Latin and etymology when choosing the name Tharpella aukensis. 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 Research (CIFAR), the US Department of Energy, Office of Science, Office of Biological and Environmental Research under award number DE-SC0016469 to VJO. DRS was supported by the Netherlands Organisation for Scientific Research, Rubicon award 019.153LW.039 and the Caltech GPS Division Texaco Postdoctoral Fellowship. FBY and SRQ were supported by the John Templeton Foundation grant 51250 and the Chan Zuckerberg Biohub. VJO 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 la Dirección General de Geografía y Medio Ambiente, Instituto Nacional de Estadística y Geografía (INEGI: Autorización EG0122018), with the associated Diplomatic Note number 18-2083 (CTC/07345/18) from la Secretaría de Relaciones Exteriores—Agencia Mexicana de Cooperación Internacional para el Desarrollo/Dirección General de Cooperación Técnica y Científica. Sample collection permit for cruise NA091 was obtained by the Ocean Exploration Trust under permit number EG0072017. Contributions: DRS and VJO conceived and designed the project. DRS, JSM, and VJO collected samples. JSM analyzed and processed cruise data. DRS, FBY, SAC, SL, and MEPS conducted experiments. DRS performed sequencing data analysis. VJO and SRQ secured funding and supervised the project. DRS wrote the original draft manuscript with input from VJO, and all authors reviewed and edited the manuscript. The authors declare no competing interests.

Attached Files

Published - s41396-022-01222-x.pdf

Supplemental Material - 41396_2022_1222_MOESM1_ESM.pdf

Supplemental Material - 41396_2022_1222_MOESM2_ESM.xlsx

Supplemental Material - 41396_2022_1222_MOESM3_ESM.xlsx

Supplemental Material - 41396_2022_1222_MOESM4_ESM.xlsx

Supplemental Material - 41396_2022_1222_MOESM5_ESM.txt

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Supplemental Material - 41396_2022_1222_MOESM8_ESM.txt

Supplemental Material - 41396_2022_1222_MOESM9_ESM.xlsx

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Additional details

Created:
August 22, 2023
Modified:
December 22, 2023