Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2023
Historique:
received: 18 01 2023
accepted: 30 07 2023
medline: 21 8 2023
pubmed: 18 8 2023
entrez: 18 8 2023
Statut: epublish

Résumé

Microbial communities in terrestrial geothermal systems often contain chemolithoautotrophs with well-characterized distributions and metabolic capabilities. However, the extent to which organic matter produced by these chemolithoautotrophs supports heterotrophs remains largely unknown. Here we compared the abundance and activity of peptidases and carbohydrate active enzymes (CAZymes) that are predicted to be extracellular identified in metagenomic assemblies from 63 springs in the Central American and the Andean convergent margin (Argentinian backarc of the Central Volcanic Zone), as well as the plume-influenced spreading center in Iceland. All assemblies contain two orders of magnitude more peptidases than CAZymes, suggesting that the microorganisms more often use proteins for their carbon and/or nitrogen acquisition instead of complex sugars. The CAZy families in highest abundance are GH23 and CBM50, and the most abundant peptidase families are M23 and C26, all four of which degrade peptidoglycan found in bacterial cells. This implies that the heterotrophic community relies on autochthonous dead cell biomass, rather than allochthonous plant matter, for organic material. Enzymes involved in the degradation of cyanobacterial- and algal-derived compounds are in lower abundance at every site, with volcanic sites having more enzymes degrading cyanobacterial compounds and non-volcanic sites having more enzymes degrading algal compounds. Activity assays showed that many of these enzyme classes are active in these samples. High temperature sites (> 80°C) had similar extracellular carbon-degrading enzymes regardless of their province, suggesting a less well-developed population of secondary consumers at these sites, possibly connected with the limited extent of the subsurface biosphere in these high temperature sites. We conclude that in < 80°C springs, chemolithoautotrophic production supports heterotrophs capable of degrading a wide range of organic compounds that do not vary by geological province, even though the taxonomic and respiratory repertoire of chemolithoautotrophs and heterotrophs differ greatly across these regions.

Identifiants

pubmed: 37594978
doi: 10.1371/journal.pone.0281277
pii: PONE-D-23-01640
pmc: PMC10437873
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0281277

Informations de copyright

Copyright: © 2023 Paul et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Raegan Paul (R)

Microbiology Department, University of Tennessee, Knoxville, TN, United States of America.

Timothy J Rogers (TJ)

Microbiology Department, University of Tennessee, Knoxville, TN, United States of America.

Kate M Fullerton (KM)

Microbiology Department, University of Tennessee, Knoxville, TN, United States of America.

Matteo Selci (M)

Department of Biology, University of Naples "Federico II", Naples, Italy.

Martina Cascone (M)

Department of Biology, University of Naples "Federico II", Naples, Italy.

Murray H Stokes (MH)

Microbiology Department, University of Tennessee, Knoxville, TN, United States of America.

Andrew D Steen (AD)

Microbiology Department, University of Tennessee, Knoxville, TN, United States of America.

J Maarten de Moor (JM)

Observatorio Volcanológico y Sismológico de Costa Rica (OVSICORI) Universidad Nacional, Heredia, Costa Rica.
Department of Earth and Planetary Sciences, University of New Mexico, Albuquerque, NM, United States of America.

Agostina Chiodi (A)

Instituto de Bio y Geociencias del NOA (IBIGEO, UNSa-CONICET), Salta, Argentina.

Andri Stefánsson (A)

NordVulk, Institute of Earth Sciences, University of Iceland, Reykjavík, Iceland.

Sæmundur A Halldórsson (SA)

NordVulk, Institute of Earth Sciences, University of Iceland, Reykjavík, Iceland.

Carlos J Ramirez (CJ)

Servicio Geologico Ambiental, Heredia, Costa Rica.

Gerdhard L Jessen (GL)

Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile.
Center for Oceanographic Research COPAS COASTAL, Universidad de Concepción, Concepción, Chile.

Peter H Barry (PH)

Marine Chemistry & Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United States of America.

Angelina Cordone (A)

Department of Biology, University of Naples "Federico II", Naples, Italy.

Donato Giovannelli (D)

Department of Biology, University of Naples "Federico II", Naples, Italy.
Marine Chemistry & Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United States of America.
National Research Council-Institute of Marine Biological Resources and Biotechnologies-CNR-IRBIM, Ancona, Italy.
Department of Marine and Coastal Science, Rutgers University, New Brunswick, NJ, United States of America.
Earth-Life Science Institute, Tokyo Institute of Technology, Tokyo, Japan.

Karen G Lloyd (KG)

Microbiology Department, University of Tennessee, Knoxville, TN, United States of America.

Classifications MeSH