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.
Highlights
Microbial heterotopic metabolism in the ocean is fueled by a supply of essential nutrients acquired via exoenzymes catalyzing depolymerization of highmolecular-weight compounds
We found the activities of leucine aminopeptidase (LAP) were inversely correlated with the dissolved inorganic nitrogen concentrations (Spearman’s rho value [rs] ϭ Ϫ0.797, P Ͻ 0.0001) (Fig. 2a)
A correlation between polysaccharide-degrading -glucosidase and protein-degrading LAP was used as an indicator of relative importance of polysaccharide- or protein-based msystems.asm.org 8
Summary
Microbial heterotopic metabolism in the ocean is fueled by a supply of essential nutrients acquired via exoenzymes catalyzing depolymerization of highmolecular-weight compounds. Sinsabaugh et al [7] showed that in soil and sediments, the production of exoenzymes is regulated by nutrient availability Factors such as pH and temperature are less significant in marine environments, and hot spots of microbial activity (e.g., marine snow) dominate the synthesis and excretion of enzymes [6, 8,9,10]. As an extension of this objective, we determine the significance of exoenzyme activities to microbial biomass and how their activities respond to factors such as available nutrients and high-molecular-weight organic substrates. As exoenzymes are one of the major toolkits microbes use for high-molecular-weight substrate degradation and resource acquisition, we predict that there will be a strong link between the enzyme activity patterns, chemical composition of the bioavailable substrates, and microbial community composition. This is true for terrestrial [16, 17] and freshwater aquatic [18] systems, but the exact mechanism of such correlations for marine ecosystems remains to be established [12,13,14,15]
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
