Kamalanathan Manoj, Doyle Shawn M, Xu Chen, Achberger Amanda M, Wade Terry L, Schwehr Kathy, Santschi Peter H, Sylvan Jason B, Quigg Antonietta
Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas, USA
Department of Oceanography, Texas A&M University, College Station, Texas, USA.
mSystems. 2020 Apr 14;5(2):e00290-20. doi: 10.1128/mSystems.00290-20.
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 (-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 -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. 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.
海洋中的微生物异位代谢是由通过外切酶催化高分子量化合物解聚而获得的必需营养物质供应所驱动的。尽管各种海洋环境中多种外切酶的活性速率已得到充分确定，但调节这些外切酶产生的因素以及在一定程度上它们与微生物群落组成的相关性却鲜为人知。本研究重点通过中宇宙实验来应对这些挑战，该实验比较了天然海水微生物群落（对照）和暴露于（油）处理的群落。β-葡萄糖苷酶、亮氨酸氨肽酶（LAP）和脂肪酶的外切酶活性与溶解营养物浓度显著相关。我们测量了碳和氮获取酶（β-葡萄糖苷酶/脂肪酶与LAP）之间的相关性，发现碳获取酶的相关性随可用初级碳源的化学性质而变化。值得注意的是，颗粒有机碳与β-葡萄糖苷酶活性之间的强相关性表明它们在多糖解聚以提供微生物生长所需碳方面的作用。最后，我们表明外切酶活性模式不一定与原核生物群落组成相关，这表明海洋微生物群落中外切酶功能的冗余性以及底物可用性。本研究为将外切酶功能与海洋系统中的溶解有机底物和下游过程联系起来提供了基础工作。微生物将外切酶释放到环境中，以将复杂的有机物和营养物质分解成可被同化和利用的更简单形式，从而满足其细胞对碳、氮和磷的需求。尽管其很重要，但与外切酶合成相关的因素尚未明确界定，特别是对于海洋环境。在这里，我们发现与氮和磷获取相关的外切酶与无机营养水平密切相关，而与碳获取相关的外切酶则取决于可用有机碳的类型。我们还展示了碳和氮获取外切酶之间的线性关系以及微生物生物量与外切酶之间的强相关性，突出了它们对微生物生产力的重要性。最后，我们表明微生物群落组成的变化与外切酶活性谱的变化没有很强的关联，这一发现揭示了微生物群落中外切酶活性功能的冗余性。这些发现推进了我们对海洋环境中与外切酶产生相关的先前未知因素的理解。
