Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions

ABSTRACT Microbial heterotopic metabolism in the ocean is fueled by a supply of essential nutrients acquired via exoenzymes catalyzing depolymerization of high-molecular-weight compounds. Although the rates of activity for a variety of exoenzymes across various marine environments are well establish...

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Autores principales:	Manoj Kamalanathan, Shawn M. Doyle, Chen Xu, Amanda M. Achberger, Terry L. Wade, Kathy Schwehr, Peter H. Santschi, Jason B. Sylvan, Antonietta Quigg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	exoenzymes nutrients oil microbial communities polysaccharides nutrient transport Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a83bb4db3e0c4bb19fd9c5ede8589e34
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spelling	oai:doaj.org-article:a83bb4db3e0c4bb19fd9c5ede8589e342021-12-02T19:47:38ZExoenzymes as a Signature of Microbial Response to Marine Environmental Conditions10.1128/mSystems.00290-202379-5077https://doaj.org/article/a83bb4db3e0c4bb19fd9c5ede8589e342020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00290-20https://doaj.org/toc/2379-5077ABSTRACT Microbial heterotopic metabolism in the ocean is fueled by a supply of essential nutrients acquired via exoenzymes catalyzing depolymerization of high-molecular-weight compounds. Although the rates of activity for a variety of exoenzymes across various marine environments are well established, the factors regulating the production of these exoenzymes, and to some extent their correlation with microbial community composition, are less known. This study focuses on addressing these challenges using a mesocosm experiment that compared a natural seawater microbial community (control) and exposed (to oil) treatment. Exoenzyme activities for β-glucosidase, leucine aminopeptidase (LAP), and lipase were significantly correlated with dissolved nutrient concentrations. We measured correlations between carbon- and nitrogen-acquiring enzymes (β-glucosidase/lipase versus LAP) and found that the correlation of carbon-acquiring enzymes varies with the chemical nature of the available primary carbon source. Notably, a strong correlation between particulate organic carbon and β-glucosidase activity demonstrates their polysaccharide depolymerization in providing the carbon for microbial growth. Last, we show that exoenzyme activity patterns are not necessarily correlated with prokaryotic community composition, suggesting a redundancy of exoenzyme functions among the marine microbial community and substrate availability. This study provides foundational work for linking exoenzyme function with dissolved organic substrate and downstream processes in marine systems. IMPORTANCE Microbes release exoenzymes into the environment to break down complex organic matter and nutrients into simpler forms that can be assimilated and utilized, thereby addressing their cellular carbon, nitrogen, and phosphorus requirements. Despite its importance, the factors associated with the synthesis of exoenzymes are not clearly defined, especially for the marine environment. Here, we found that exoenzymes associated with nitrogen and phosphorus acquisition were strongly correlated with inorganic nutrient levels, while those associated with carbon acquisition depended on the type of organic carbon available. We also show a linear relationship between carbon- and nitrogen-acquiring exoenzymes and a strong correlation between microbial biomass and exoenzymes, highlighting their significance to microbial productivity. Last, we show that changes in microbial community composition are not strongly associated with changes in exoenzyme activity profiles, a finding which reveals a redundancy of exoenzyme activity functions among microbial community. These findings advance our understanding of previously unknown factors associated with exoenzyme production in the marine environment.Manoj KamalanathanShawn M. DoyleChen XuAmanda M. AchbergerTerry L. WadeKathy SchwehrPeter H. SantschiJason B. SylvanAntonietta QuiggAmerican Society for Microbiologyarticleexoenzymesnutrientsoilmicrobial communitiespolysaccharidesnutrient transportMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	exoenzymes nutrients oil microbial communities polysaccharides nutrient transport Microbiology QR1-502
spellingShingle	exoenzymes nutrients oil microbial communities polysaccharides nutrient transport Microbiology QR1-502 Manoj Kamalanathan Shawn M. Doyle Chen Xu Amanda M. Achberger Terry L. Wade Kathy Schwehr Peter H. Santschi Jason B. Sylvan Antonietta Quigg Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions
description	ABSTRACT Microbial heterotopic metabolism in the ocean is fueled by a supply of essential nutrients acquired via exoenzymes catalyzing depolymerization of high-molecular-weight compounds. Although the rates of activity for a variety of exoenzymes across various marine environments are well established, the factors regulating the production of these exoenzymes, and to some extent their correlation with microbial community composition, are less known. This study focuses on addressing these challenges using a mesocosm experiment that compared a natural seawater microbial community (control) and exposed (to oil) treatment. Exoenzyme activities for β-glucosidase, leucine aminopeptidase (LAP), and lipase were significantly correlated with dissolved nutrient concentrations. We measured correlations between carbon- and nitrogen-acquiring enzymes (β-glucosidase/lipase versus LAP) and found that the correlation of carbon-acquiring enzymes varies with the chemical nature of the available primary carbon source. Notably, a strong correlation between particulate organic carbon and β-glucosidase activity demonstrates their polysaccharide depolymerization in providing the carbon for microbial growth. Last, we show that exoenzyme activity patterns are not necessarily correlated with prokaryotic community composition, suggesting a redundancy of exoenzyme functions among the marine microbial community and substrate availability. This study provides foundational work for linking exoenzyme function with dissolved organic substrate and downstream processes in marine systems. IMPORTANCE Microbes release exoenzymes into the environment to break down complex organic matter and nutrients into simpler forms that can be assimilated and utilized, thereby addressing their cellular carbon, nitrogen, and phosphorus requirements. Despite its importance, the factors associated with the synthesis of exoenzymes are not clearly defined, especially for the marine environment. Here, we found that exoenzymes associated with nitrogen and phosphorus acquisition were strongly correlated with inorganic nutrient levels, while those associated with carbon acquisition depended on the type of organic carbon available. We also show a linear relationship between carbon- and nitrogen-acquiring exoenzymes and a strong correlation between microbial biomass and exoenzymes, highlighting their significance to microbial productivity. Last, we show that changes in microbial community composition are not strongly associated with changes in exoenzyme activity profiles, a finding which reveals a redundancy of exoenzyme activity functions among microbial community. These findings advance our understanding of previously unknown factors associated with exoenzyme production in the marine environment.
format	article
author	Manoj Kamalanathan Shawn M. Doyle Chen Xu Amanda M. Achberger Terry L. Wade Kathy Schwehr Peter H. Santschi Jason B. Sylvan Antonietta Quigg
author_facet	Manoj Kamalanathan Shawn M. Doyle Chen Xu Amanda M. Achberger Terry L. Wade Kathy Schwehr Peter H. Santschi Jason B. Sylvan Antonietta Quigg
author_sort	Manoj Kamalanathan
title	Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions
title_short	Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions
title_full	Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions
title_fullStr	Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions
title_full_unstemmed	Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions
title_sort	exoenzymes as a signature of microbial response to marine environmental conditions
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/a83bb4db3e0c4bb19fd9c5ede8589e34
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_version_	1718375981688815616

Exoenzymes as a Signature of Microbial Response to Marine Environmental Conditions

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