Metagenome-assembled genomes of deep-sea sediments: changes in microbial functional potential lag behind redox transitions

Type Article
Date 2024-01
Language English
Author(s) Schauberger ClemensORCID1, Thamdrup BoORCID1, Lemonnier ClarisseORCID2, Trouche BlandineORCID2, Poulain JulieORCID3, 4, Wincker PatrickORCID3, 4, Arnaud-Haond SophieORCID5, Glud Ronnie NORCID1, 6, Maignien LoisORCID2
Affiliation(s) 1 : Department of Biology, University of Southern Denmark , 5230 Odense M, Denmark
2 : Univ Brest, CNRS, IFREMER, Microbiology of Extreme Environments Laboratory , F-29280 Plouzané, France
3 : Génomique Métabolique , Genoscope, Evry, France
4 : Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay , Genoscope, Evry, France
5 : MARBEC, Institut Français de Recherche pour L'Exploitation de la Mer, Univ Montpellier, CNRS, IRD , Sète, France
6 : Department of Ocean and Environmental Sciences, Tokyo University of Marine Science and Technology , Tokyo, Japan
Source Isme Communications (2730-6151) (Oxford University Press (OUP)), 2024-01 , Vol. 4 , N. 1 , P. ycad005 (13p.)
DOI 10.1093/ismeco/ycad005
Keyword(s) microbial ecology, geomicrobiology, marine sediments, hadal zone, metagenomics, redox gradients, biogeochemistry, CAZymes
Abstract

Hadal sediments are hotspots of microbial activity in the deep-sea and exhibit strong biogeochemical gradients. But while these gradients are widely assumed to exert selective forces on hadal microbial communities, the actual relationship between biogeochemistry, functional traits, and microbial community structure remains poorly understood. We tested whether the biogeochemical conditions in hadal sediments select for microbes based on their genomic capacity for respiration and carbohydrate utilization via a metagenomic analysis of over 153 samples from the Atacama Trench region (max. Depth 8085 m). The obtained 1357 non-redundant microbial genomes were affiliated with about one third of all known microbial phyla, with more than half belonging to unknown genera. This indicated that the capability to withstand extreme hydrostatic pressure is a phylogenetically widespread trait and that hadal sediments are inhabited by diverse microbial lineages. While community composition changed gradually over sediment depth, these changes were not driven by selection for respiratory or carbohydrate degradation capability in the oxic and nitrogenous zones, except in the case of anammox bacteria and nitrifying archaea. However, selection based on respiration and carbohydrate degradation capacity did structure the communities of the ferruginous zone, where aerobic and nitrogen respiring microbes declined exponentially (half-life 125–419 years) and were replaced by subsurface communities. These results highlight a delayed response of microbial community composition to selective pressure imposed by redox zonation and indicated that gradual changes in microbial composition are shaped by the high-resilience and slow growth of microbes in the seafloor.

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Schauberger Clemens, Thamdrup Bo, Lemonnier Clarisse, Trouche Blandine, Poulain Julie, Wincker Patrick, Arnaud-Haond Sophie, Glud Ronnie N, Maignien Lois (2024). Metagenome-assembled genomes of deep-sea sediments: changes in microbial functional potential lag behind redox transitions. Isme Communications, 4(1), ycad005 (13p.). Publisher's official version : https://doi.org/10.1093/ismeco/ycad005 , Open Access version : https://archimer.ifremer.fr/doc/00871/98285/