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 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.

Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column

“…It also indicates that the rates of hydrocarbon degradation in BOMAs may be important in comparison to rates among free-living microorganisms. These findings are the first to link BOMAs to hydrocarbon degradation and are consistent with research showing marine snow and other biomass aggregates are hot spots for microbial activity ( 28 , 31 – 33 ).…”

GoMRI Insights into Microbial Genomics and Hydrocarbon Bioremediation Response in Marine Ecosystems

“…Coastal nitrifier populations in offshore pelagic waters underwent alteration in species composition for at least a year, returning to normal only after the oil had dissipated. (Newell et al, 2014;Huettel et al, 2018) Community composition shifted over time as hydrocarbon oxidizing bacterial blooms consumed available hydrocarbons, and then declined, being replaced by microbial species capable of degrading the residual metabolic byproducts (Figure 1; Kostka et al, 2011;Rodriguez-R et al, 2015;Kamalanathan et al, 2020). Such microbial succession patterns have FIGURE 1 (NEXT PAGE).…”

Aggregation and Degradation of Dispersants and Oil by Microbial Exopolymers (ADDOMEx): Toward a Synthesis of Processes and Pathways of Marine Oil Snow Formation in Determining the Fate of Hydrocarbons

“…has amphiphilic properties, thereby interacting easily with hydrophobic substrates like hydrocarbons, leading to the solubilization and biodegradation of oil components (Gutierrez et al, 2013a). The exopolymer concentrations with entrained oil droplets grow to form networks that also act as an energy and carbon source to other members of the microbial community (Sinsabaugh et al, 2009;Kamalanathan et al, 2020). In addition, the production of EPS may facilitate attachment of specific microbes (e.g., Pseudomonas putida) to polycyclic aromatic hydrocarbons (McGenity et al, 2012).…”