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Life strategies for Aminicenantia in subseafloor oceanic crust

The ISME Journal volume 17, pages 1406–1415 (2023)Cite this article

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Abstract

After decades studying the microbial “deep biosphere” in subseafloor oceanic crust, the growth and life strategies in this anoxic, low energy habitat remain poorly described. Using both single cell genomics and metagenomics, we reveal the life strategies of two distinct lineages of uncultivated Aminicenantia bacteria from the basaltic subseafloor oceanic crust of the eastern flank of the Juan de Fuca Ridge. Both lineages appear adapted to scavenge organic carbon, as each have genetic potential to catabolize amino acids and fatty acids, aligning with previous Aminicenantia reports. Given the organic carbon limitation in this habitat, seawater recharge and necromass may be important carbon sources for heterotrophic microorganisms inhabiting the ocean crust. Both lineages generate ATP via several mechanisms including substrate-level phosphorylation, anaerobic respiration, and electron bifurcation driving an Rnf ion translocation membrane complex. Genomic comparisons suggest these Aminicenantia transfer electrons extracellularly, perhaps to iron or sulfur oxides consistent with mineralogy of this site. One lineage, called JdFR-78, has small genomes that are basal to the Aminicenantia class and potentially use “primordial” siroheme biosynthetic intermediates for heme synthesis, suggesting this lineage retain characteristics of early evolved life. Lineage JdFR-78 contains CRISPR-Cas defenses to evade viruses, while other lineages contain prophage that may help prevent super-infection or no detectable viral defenses. Overall, genomic evidence points to Aminicenantia being well adapted to oceanic crust environments by taking advantage of simple organic molecules and extracellular electron transport.

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Fig. 1: Aminicenantia 16S rRNA gene phylogenetic tree reveals two lineages living in the Juan de Fuca Ridge flank oceanic crust.
Fig. 2: Carbon utilization and energy generation metabolisms within the Juan de Fuca Aminicenantia.
Fig. 3: Comparison of CRISPR arrays in Juan de Fuca crustal fluid Aminicenantia.
Fig. 4: Genomic and phylogenomic properties of Aminicenantia order JdFR-78 indicate evolutionary differences.
Fig. 5: Life strategies for two lineages of Aminicenantia living in the warm and anoxic crustal fluids of the Juan de Fuca Ridge flank.

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Data availability

All SAG data for this project can be found on NCBI under BioProject ID PRJNA842252 under accession numbers: JAMZRZ000000000 (JDF1 composite genome); JAMZSA000000000 (AH-873-B07); JAMZSB000000000 (AC-708-M15); JAMZSC000000000 (AC-708-I09); JAMZSD000000000 (AC-335-O07); JAMZSE000000000 (AC-335-L06); JAMZSF000000000 (AC-335-K20); JAMZSG000000000 (AC-335-G13); JAMZSH000000000 (AC-335-B20); JAMZSI000000000 (AC-335-A11); JAMZSJ000000000 (AC-334-K16); JAMZSK000000000 (AC-334-E05). All MAG data for this project can be found on IMG.

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Acknowledgements

The authors thank the science parties and crews of expeditions AT18-07, AT26-18 and AT42-11 for their support to collect the samples used in this study. We also thank Jennifer Gladstone, Anna Chen, Melody Lindsay and Julia McGonigle for discussions that helped shape the direction of this study, the staff of the Single Cell Genomics Center at the Bigelow Laboratory for Ocean Science and the Joint Genome Institute (JGI) for all sequencing, and Ruth Booker and Orion Thomas for extensive proof-reading. Samples from 2019 were collected with the consent of the Government of Canada, as reviewed by Global Affairs Canada.

Funding

Funding for the expeditions was provided by the U.S. National Science Foundation (awards OCE-1260723 to MSR, OCE-1260548 to C. Geoff Wheat, and OCE-1737017 to BNO). Funding for analyses was provided in part from the NSF (award OCE-173017 to BNO, OCE-1851582 to MSR, and OIA-1826734 to RS and BNO), from the NASA Exobiology program (80NSSC19K0466 to BNO), from the Center for Dark Energy Biosphere Investigation (C-DEBI; subaward from OCE-0939654 to BNO), and from the Rodney White Fellowship provided by Bigelow Laboratory for Ocean Sciences (to AEB and AAB). The work conducted by the US Department of Energy JGI, a US Department of Energy Office of Science User Facility, is supported under contract no. DE-AC02-05CH11231. This is HIMB contribution number 1933 and SOEST contribution number 11682.

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Authors and Affiliations

  1. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA

    Anne E. Booker, Timothy D’Angelo, Annabelle Adams-Beyea, Julia M. Brown, Ramunas Stepanauskas & Beth N. Orcutt

  2. Eugene Lang College of Liberal Arts at The New School, New York City, NY, USA

    Annabelle Adams-Beyea

  3. Department of Natural Science, Hawaiʻi Pacific University, Honolulu, HI, USA

    Olivia Nigro

  4. Hawaiʻi Institute of Marine Biology, SOEST, University of Hawaiʻi at Mānoa, Kāneʻohe, HI, USA

    Michael S. Rappé

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  1. Anne E. Booker
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  8. Beth N. Orcutt
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Contributions

AEB, BNO, JMB, and TD conceived the project and designed the analyses. BNO, MSR, and RS secured funding. AEB, TD, AAB, JMB performed the analyses. All authors interpreted the results and wrote the manuscript.

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Correspondence to Beth N. Orcutt.

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Booker, A.E., D’Angelo, T., Adams-Beyea, A. et al. Life strategies for Aminicenantia in subseafloor oceanic crust. ISME J 17, 1406–1415 (2023). https://doi.org/10.1038/s41396-023-01454-5

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