Abstract
The factors and processes that influence the behavior and functionality of ecosystems inhabited by complex microbiomes are still far from being clearly understood. Synthetic microbial communities provide reduced-complexity models that allow an examination of ecological theories under defined and controlled conditions. In this study, we applied a multiphasic approach to study synthetic methane-oxidizing communities and species interactions as proxies to the natural communities. Our results confirm that, under selective pressures, natural-sediment communities of high complexity simplify rapidly, selecting for several major functional guilds, the major partners in methane oxidation being the Methylococcaceae methanotrophs and the Methylophilaceae methylotrophs, along with minor but persistent partners, members of Burkholderiales and Flavobacteriales As a proof of concept, we established minimalist synthetic communities that were representative of the four functional guilds to demonstrate the dependency of the non-methane-utilizing species on the methanotrophs as the primary carbon-providing species. We observed that in communities consisting of multiple representatives of the key guilds, members of the same guild appeared to compete for resources. For example, when two methanotrophs of the same family were present, the two expressed similar key methanotrophy pathways and responded similarly to changing environmental conditions, suggesting that they perform a similar keystone function in situ Similar observations were made for the Methylophilaceae However, differences were noted in the expression of auxiliary and unique genes among strains of the same functional guild, reflecting differential adaptation and suggesting mechanisms for competition. At the same time, differences were also noted in the performances of partners with specific metabolic schemes. For example, a mutant of Methylotenera mobilis impaired in nitrate utilization behaved as a more efficient cooperator in methane consumption, suggesting that the loss of function may lead to changes in communal behavior. Overall, we demonstrate the robust nature of synthetic communities built of native lake sediment strains and their utility in addressing important ecological questions while using a simplified model.IMPORTANCE The metabolism of methane is an important part of the global carbon cycle. While deciphering the community function and the potential role of the different functional guilds is very difficult when considering native complex communities, synthetic communities, built of species originating from a study site in question, present a simplified model and allow specific questions to be addressed as to carbon, nitrogen, and other nutrient transfer among species in a controlled system. This study applies an ecophysiological approach, as a proof of principle, to an already well-studied model system, contributing to a better understanding of microbial community function and microbial ecosystem processes.
Highlights
The factors and processes that influence the behavior and functionality of ecosystems inhabited by complex microbiomes are still far from being clearly understood
The major functional guild of microbes involved in methane consumption in these environments is the aerobic methane-oxidizing bacteria, whose activity constitutes a natural filter that mitigates the escape of methane into the atmosphere [10]
In addition to the previously noted dominant community members, the Methylococcaceae and the Methylophilaceae [18,19,20], we noted the minor but persistent presence of two additional functional guilds, bacteria of the orders Burkholderiales and Flavobacteriales, suggesting that carbon from methane may be transferred beyond Methylophilaceae methylotrophs to a broader community (Fig. 1)
Summary
The factors and processes that influence the behavior and functionality of ecosystems inhabited by complex microbiomes are still far from being clearly understood. The factors and processes that influence the behavior and functionality of a methaneoxidizing microbiome are hard to elucidate when using in situ experiments due the complexity of the natural communities, the unpredictable changes in community structure due to uncontrollable factors such as predation, the heterogeneity of organisms representing major functional guilds, and the interconnected nature of biogeochemical cycles. In this regard, a model synthetic system that links function to identity can help elucidate the relationships between microorganisms and ecosystem processes [11, 12]. Partnership, and role of competition in these synthetic communities, flow cytometry, metagenomics, metatranscriptomics, and stable isotope DNA labeling were employed
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