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The ecology of microbial metabolic pathways Louca, Stilianos

Abstract

Microbial metabolic activity drives biogeochemical cycling in virtually every ecosystem. Yet, microbial ecology and its role in ecosystem biochemistry remain poorly understood, partly because the enormous diversity found in microbial communities hinders their modeling. Despite this diversity, the bulk of global biogeochemical fluxes is driven by a few metabolic pathways encoded by a small set of genes, which through time have spread across microbial clades that can replace each other within metabolic niches. Hence, the question arises whether the dynamics of these pathways can be modeled regardless of the hosting organisms, for example based on environmental conditions. Such a pathway-centric paradigm would greatly simplify the modeling of microbial processes at ecosystem scales. Here I investigate the applicability of a pathway-centric paradigm for microbial ecology. By examining microbial communities in replicate "miniature" aquatic environments, I show that similar ecosystems can exhibit similar metabolic functional community structure, despite highly variable taxonomic composition within individual functional groups. Further, using data from a recent ocean survey I show that environmental conditions strongly explain the distribution of microbial metabolic functional groups across the world's oceans, but only poorly explain the taxonomic composition within individual functional groups. Using statistical tools and mathematical models I conclude that biotic interactions, such as competition and predation, likely underlie much of the taxonomic variation within functional groups observed in the aforementioned studies. The above findings strongly support a pathway-centric paradigm, in which the distribution and activity of microbial metabolic pathways is strongly determined by energetic and stoichiometric constraints, whereas additional mechanisms shape the taxonomic composition within metabolic guilds. These findings motivated me to explore concrete pathway-centric mathematical models for specific ecosystems. Notably, I constructed a biogeochemical model for Saanich Inlet, a seasonally anoxic fjord with biogeochemistry analogous to oxygen minimum zones. The model describes the dynamics of individual microbial metabolic pathways involved in carbon, nitrogen and sulfur cycling, and largely explains geochemical depth profiles as well as DNA, mRNA and protein sequence data. This work yields insight into ocean biogeochemistry and demonstrates the potential of pathway-centric models for microbial ecology.

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