Cargando…

Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea

Heterotrophic microorganisms in marine sediments produce extracellular enzymes to hydrolyze organic macromolecules, so their products can be transported inside the cell and used for energy and growth. Therefore, extracellular enzymes may mediate the fate of organic carbon in sediments. The Baltic Se...

Descripción completa

Detalles Bibliográficos
Autores principales: Schmidt, Jenna M., Royalty, Taylor M., Lloyd, Karen G., Steen, Andrew D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8485070/
https://www.ncbi.nlm.nih.gov/pubmed/34603228
http://dx.doi.org/10.3389/fmicb.2021.702015
_version_ 1784577459985842176
author Schmidt, Jenna M.
Royalty, Taylor M.
Lloyd, Karen G.
Steen, Andrew D.
author_facet Schmidt, Jenna M.
Royalty, Taylor M.
Lloyd, Karen G.
Steen, Andrew D.
author_sort Schmidt, Jenna M.
collection PubMed
description Heterotrophic microorganisms in marine sediments produce extracellular enzymes to hydrolyze organic macromolecules, so their products can be transported inside the cell and used for energy and growth. Therefore, extracellular enzymes may mediate the fate of organic carbon in sediments. The Baltic Sea Basin is a primarily depositional environment with high potential for organic matter preservation. The potential activities of multiple organic carbon-degrading enzymes were measured in samples obtained by the International Ocean Discovery Program Expedition 347 from the Little Belt Strait, Denmark, core M0059C. Potential maximum hydrolysis rates (V(max)) were measured at depths down to 77.9mbsf for the following enzymes: alkaline phosphatase, β-d-xylosidase, β-d-cellobiohydrolase, N-acetyl-β-d-glucosaminidase, β-glucosidase, α-glucosidase, leucyl aminopeptidase, arginyl aminopeptidase, prolyl aminopeptidase, gingipain, and clostripain. Extracellular peptidase activities were detectable at depths shallower than 54.95mbsf, and alkaline phosphatase activity was detectable throughout the core, albeit against a relatively high activity in autoclaved sediments. β-glucosidase activities were detected above 30mbsf; however, activities of other glycosyl hydrolases (β-xylosidase, β-cellobiohydrolase, N-acetyl-β-glucosaminidase, and α-glucosidase) were generally indistinguishable from zero at all depths. These extracellular enzymes appear to be extremely stable: Among all enzymes, a median of 51.3% of enzyme activity was retained after autoclaving for an hour. We show that enzyme turnover times scale with the inverse of community metabolic rates, such that enzyme lifetimes in subsurface sediments, in which metabolic rates are very slow, are likely to be extraordinarily long. A back-of-the-envelope calculation suggests enzyme lifetimes are, at minimum, on the order of 230days, and may be substantially longer. These results lend empirical support to the hypothesis that a population of subsurface microbes persist by using extracellular enzymes to slowly metabolize old, highly degraded organic carbon.
format Online
Article
Text
id pubmed-8485070
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-84850702021-10-02 Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea Schmidt, Jenna M. Royalty, Taylor M. Lloyd, Karen G. Steen, Andrew D. Front Microbiol Microbiology Heterotrophic microorganisms in marine sediments produce extracellular enzymes to hydrolyze organic macromolecules, so their products can be transported inside the cell and used for energy and growth. Therefore, extracellular enzymes may mediate the fate of organic carbon in sediments. The Baltic Sea Basin is a primarily depositional environment with high potential for organic matter preservation. The potential activities of multiple organic carbon-degrading enzymes were measured in samples obtained by the International Ocean Discovery Program Expedition 347 from the Little Belt Strait, Denmark, core M0059C. Potential maximum hydrolysis rates (V(max)) were measured at depths down to 77.9mbsf for the following enzymes: alkaline phosphatase, β-d-xylosidase, β-d-cellobiohydrolase, N-acetyl-β-d-glucosaminidase, β-glucosidase, α-glucosidase, leucyl aminopeptidase, arginyl aminopeptidase, prolyl aminopeptidase, gingipain, and clostripain. Extracellular peptidase activities were detectable at depths shallower than 54.95mbsf, and alkaline phosphatase activity was detectable throughout the core, albeit against a relatively high activity in autoclaved sediments. β-glucosidase activities were detected above 30mbsf; however, activities of other glycosyl hydrolases (β-xylosidase, β-cellobiohydrolase, N-acetyl-β-glucosaminidase, and α-glucosidase) were generally indistinguishable from zero at all depths. These extracellular enzymes appear to be extremely stable: Among all enzymes, a median of 51.3% of enzyme activity was retained after autoclaving for an hour. We show that enzyme turnover times scale with the inverse of community metabolic rates, such that enzyme lifetimes in subsurface sediments, in which metabolic rates are very slow, are likely to be extraordinarily long. A back-of-the-envelope calculation suggests enzyme lifetimes are, at minimum, on the order of 230days, and may be substantially longer. These results lend empirical support to the hypothesis that a population of subsurface microbes persist by using extracellular enzymes to slowly metabolize old, highly degraded organic carbon. Frontiers Media S.A. 2021-09-17 /pmc/articles/PMC8485070/ /pubmed/34603228 http://dx.doi.org/10.3389/fmicb.2021.702015 Text en Copyright © 2021 Schmidt, Royalty, Lloyd and Steen. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Schmidt, Jenna M.
Royalty, Taylor M.
Lloyd, Karen G.
Steen, Andrew D.
Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea
title Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea
title_full Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea
title_fullStr Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea
title_full_unstemmed Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea
title_short Potential Activities and Long Lifetimes of Organic Carbon-Degrading Extracellular Enzymes in Deep Subsurface Sediments of the Baltic Sea
title_sort potential activities and long lifetimes of organic carbon-degrading extracellular enzymes in deep subsurface sediments of the baltic sea
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8485070/
https://www.ncbi.nlm.nih.gov/pubmed/34603228
http://dx.doi.org/10.3389/fmicb.2021.702015
work_keys_str_mv AT schmidtjennam potentialactivitiesandlonglifetimesoforganiccarbondegradingextracellularenzymesindeepsubsurfacesedimentsofthebalticsea
AT royaltytaylorm potentialactivitiesandlonglifetimesoforganiccarbondegradingextracellularenzymesindeepsubsurfacesedimentsofthebalticsea
AT lloydkareng potentialactivitiesandlonglifetimesoforganiccarbondegradingextracellularenzymesindeepsubsurfacesedimentsofthebalticsea
AT steenandrewd potentialactivitiesandlonglifetimesoforganiccarbondegradingextracellularenzymesindeepsubsurfacesedimentsofthebalticsea