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

Autores
Paul, Raegan; Rogers, Timothy J.; Fullerton, Kate M.; Selci, Matteo; Cascone, Martina; Stokes, Murray H.; Steen, Andrew D.; de Moor, J. Maarten; Chiodi, Agostina Laura; Stefánsson, Andri; Halldórsson, Sæmundur A.; Ramirez, Carlos J.; Jessen, Gerdhard L.; Barry, Peter H.; Cordone, Angelina; Giovannelli, Donato; Lloyd, Karen G.
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Paul, Raegan. University of Tennessee; Estados Unidos
Fil: Rogers, Timothy J.. University of Tennessee; Estados Unidos
Fil: Fullerton, Kate M.. University of Tennessee; Estados Unidos
Fil: Selci, Matteo. Università degli Studi di Napoli Federico II; Italia
Fil: Cascone, Martina. Università degli Studi di Napoli Federico II; Italia
Fil: Stokes, Murray H.. University of Tennessee; Estados Unidos
Fil: Steen, Andrew D.. University of Tennessee; Estados Unidos
Fil: de Moor, J. Maarten. University of New Mexico; Estados Unidos
Fil: Chiodi, Agostina Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Salta. Instituto de Bio y Geociencias del NOA. Universidad Nacional de Salta. Facultad de Ciencias Naturales. Museo de Ciencias Naturales. Instituto de Bio y Geociencias del NOA; Argentina
Fil: Stefánsson, Andri. University of Iceland; Islandia
Fil: Halldórsson, Sæmundur A.. University of Iceland; Islandia
Fil: Ramirez, Carlos J.. Servicio Geológico Ambiental; Costa Rica
Fil: Jessen, Gerdhard L.. Universidad de Concepción; Chile
Fil: Barry, Peter H.. No especifíca;
Fil: Cordone, Angelina. Università degli Studi di Napoli Federico II; Italia
Fil: Giovannelli, Donato. Consiglio Nazionale delle Ricerche; Italia. Università degli Studi di Napoli Federico II; Italia
Fil: Lloyd, Karen G.. University of Tennessee; Estados Unidos
Materia
MICROBIAL COMMUNITIES
GEOTHERMAL FLUIDS
CONVERGENT MARGIN
CARBON BUDGET
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/230278

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oai_identifier_str oai:ri.conicet.gov.ar:11336/230278
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystemsPaul, RaeganRogers, Timothy J.Fullerton, Kate M.Selci, MatteoCascone, MartinaStokes, Murray H.Steen, Andrew D.de Moor, J. MaartenChiodi, Agostina LauraStefánsson, AndriHalldórsson, Sæmundur A.Ramirez, Carlos J.Jessen, Gerdhard L.Barry, Peter H.Cordone, AngelinaGiovannelli, DonatoLloyd, Karen G.MICROBIAL COMMUNITIESGEOTHERMAL FLUIDSCONVERGENT MARGINCARBON BUDGEThttps://purl.org/becyt/ford/1.5https://purl.org/becyt/ford/1Microbial 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.Fil: Paul, Raegan. University of Tennessee; Estados UnidosFil: Rogers, Timothy J.. University of Tennessee; Estados UnidosFil: Fullerton, Kate M.. University of Tennessee; Estados UnidosFil: Selci, Matteo. Università degli Studi di Napoli Federico II; ItaliaFil: Cascone, Martina. Università degli Studi di Napoli Federico II; ItaliaFil: Stokes, Murray H.. University of Tennessee; Estados UnidosFil: Steen, Andrew D.. University of Tennessee; Estados UnidosFil: de Moor, J. Maarten. University of New Mexico; Estados UnidosFil: Chiodi, Agostina Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Salta. Instituto de Bio y Geociencias del NOA. Universidad Nacional de Salta. Facultad de Ciencias Naturales. Museo de Ciencias Naturales. Instituto de Bio y Geociencias del NOA; ArgentinaFil: Stefánsson, Andri. University of Iceland; IslandiaFil: Halldórsson, Sæmundur A.. University of Iceland; IslandiaFil: Ramirez, Carlos J.. Servicio Geológico Ambiental; Costa RicaFil: Jessen, Gerdhard L.. Universidad de Concepción; ChileFil: Barry, Peter H.. No especifíca;Fil: Cordone, Angelina. Università degli Studi di Napoli Federico II; ItaliaFil: Giovannelli, Donato. Consiglio Nazionale delle Ricerche; Italia. Università degli Studi di Napoli Federico II; ItaliaFil: Lloyd, Karen G.. University of Tennessee; Estados UnidosPublic Library of Science2023-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/230278Paul, Raegan; Rogers, Timothy J.; Fullerton, Kate M.; Selci, Matteo; Cascone, Martina; et al.; Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems; Public Library of Science; Plos One; 18; 8-2023; 1-261932-6203CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0281277info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:03:33Zoai:ri.conicet.gov.ar:11336/230278instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:03:33.463CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
title Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
spellingShingle Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
Paul, Raegan
MICROBIAL COMMUNITIES
GEOTHERMAL FLUIDS
CONVERGENT MARGIN
CARBON BUDGET
title_short Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
title_full Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
title_fullStr Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
title_full_unstemmed Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
title_sort Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems
dc.creator.none.fl_str_mv Paul, Raegan
Rogers, Timothy J.
Fullerton, Kate M.
Selci, Matteo
Cascone, Martina
Stokes, Murray H.
Steen, Andrew D.
de Moor, J. Maarten
Chiodi, Agostina Laura
Stefánsson, Andri
Halldórsson, Sæmundur A.
Ramirez, Carlos J.
Jessen, Gerdhard L.
Barry, Peter H.
Cordone, Angelina
Giovannelli, Donato
Lloyd, Karen G.
author Paul, Raegan
author_facet Paul, Raegan
Rogers, Timothy J.
Fullerton, Kate M.
Selci, Matteo
Cascone, Martina
Stokes, Murray H.
Steen, Andrew D.
de Moor, J. Maarten
Chiodi, Agostina Laura
Stefánsson, Andri
Halldórsson, Sæmundur A.
Ramirez, Carlos J.
Jessen, Gerdhard L.
Barry, Peter H.
Cordone, Angelina
Giovannelli, Donato
Lloyd, Karen G.
author_role author
author2 Rogers, Timothy J.
Fullerton, Kate M.
Selci, Matteo
Cascone, Martina
Stokes, Murray H.
Steen, Andrew D.
de Moor, J. Maarten
Chiodi, Agostina Laura
Stefánsson, Andri
Halldórsson, Sæmundur A.
Ramirez, Carlos J.
Jessen, Gerdhard L.
Barry, Peter H.
Cordone, Angelina
Giovannelli, Donato
Lloyd, Karen G.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv MICROBIAL COMMUNITIES
GEOTHERMAL FLUIDS
CONVERGENT MARGIN
CARBON BUDGET
topic MICROBIAL COMMUNITIES
GEOTHERMAL FLUIDS
CONVERGENT MARGIN
CARBON BUDGET
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.5
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: Paul, Raegan. University of Tennessee; Estados Unidos
Fil: Rogers, Timothy J.. University of Tennessee; Estados Unidos
Fil: Fullerton, Kate M.. University of Tennessee; Estados Unidos
Fil: Selci, Matteo. Università degli Studi di Napoli Federico II; Italia
Fil: Cascone, Martina. Università degli Studi di Napoli Federico II; Italia
Fil: Stokes, Murray H.. University of Tennessee; Estados Unidos
Fil: Steen, Andrew D.. University of Tennessee; Estados Unidos
Fil: de Moor, J. Maarten. University of New Mexico; Estados Unidos
Fil: Chiodi, Agostina Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Salta. Instituto de Bio y Geociencias del NOA. Universidad Nacional de Salta. Facultad de Ciencias Naturales. Museo de Ciencias Naturales. Instituto de Bio y Geociencias del NOA; Argentina
Fil: Stefánsson, Andri. University of Iceland; Islandia
Fil: Halldórsson, Sæmundur A.. University of Iceland; Islandia
Fil: Ramirez, Carlos J.. Servicio Geológico Ambiental; Costa Rica
Fil: Jessen, Gerdhard L.. Universidad de Concepción; Chile
Fil: Barry, Peter H.. No especifíca;
Fil: Cordone, Angelina. Università degli Studi di Napoli Federico II; Italia
Fil: Giovannelli, Donato. Consiglio Nazionale delle Ricerche; Italia. Università degli Studi di Napoli Federico II; Italia
Fil: Lloyd, Karen G.. University of Tennessee; Estados Unidos
description 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.
publishDate 2023
dc.date.none.fl_str_mv 2023-08
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/230278
Paul, Raegan; Rogers, Timothy J.; Fullerton, Kate M.; Selci, Matteo; Cascone, Martina; et al.; Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems; Public Library of Science; Plos One; 18; 8-2023; 1-26
1932-6203
CONICET Digital
CONICET
url http://hdl.handle.net/11336/230278
identifier_str_mv Paul, Raegan; Rogers, Timothy J.; Fullerton, Kate M.; Selci, Matteo; Cascone, Martina; et al.; Complex organic matter degradation by secondary consumers in chemolithoautotrophy-based subsurface geothermal ecosystems; Public Library of Science; Plos One; 18; 8-2023; 1-26
1932-6203
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0281277
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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