Abstract

Cycles of nutrients (N, P, etc.) and resources (C) are a defining emergent feature of ecosystems. Cycling plays a critical role in determining ecosystem structure at all scales, from microbial communities to the entire biosphere. Stable cycles are essential for ecosystem persistence because they allow resources and nutrients to be regenerated. Therefore, a central problem in ecology is understanding how ecosystems are organized to sustain robust cycles. Addressing this problem quantitatively has proved challenging because of the difficulties associated with manipulating ecosystem structure while measuring cycling. We address this problem using closed microbial ecosystems (CES), hermetically sealed microbial consortia provided with only light. We develop a technique for quantifying carbon cycling in hermetically sealed microbial communities and show that CES composed of an alga and diverse bacterial consortia self-organize to robustly cycle carbon for months. Comparing replicates of diverse CES, we find that carbon cycling does not depend strongly on the taxonomy of the bacteria present. Moreover, despite strong taxonomic differences, self-organized CES exhibit a conserved set of metabolic capabilities. Therefore, an emergent carbon cycle enforces metabolic but not taxonomic constraints on ecosystem organization. Our study helps establish closed microbial communities as model ecosystems to study emergent function and persistence in replicate systems while controlling community composition and the environment.

Highlights

  • Cycles of nutrients (N, P, etc.) and resources (C) are a defining emergent feature of ecosystems

  • Enabled by a new high-precision method to quantify carbon cycling, we show that materially closed microbial ecosystems (CES) provided with only light self-organize to robustly cycle carbon

  • We cannot detect carbon cycling from C. reinhardtii alone (

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Summary

BIOPHYSICS AND COMPUTATIONAL BIOLOGY

Luis Miguel de Jesús Astacioa,b,1 , Kaumudi H. A primary roadblock to studying nutrient cycling in model microbial communities is experimental: Most existing approaches use batch [9] or continuous culture [11], where nutrients are supplied externally at high rates In these conditions, nutrient cycling rarely occurs since the external supply of nutrients favors those strains that can most rapidly exploit the supplied resource [8, 9]. We seek to overcome some of the limitations of existing methods by establishing closed microbial ecosystems (CES) as model systems for understanding how communities are assembled to cycle nutrients. We hope that CES can complement existing batch-culture, chemostat, and Winogradsky column-based approaches [18]

Closed Microbial Communities
Carbon Cycling in Closed Microbial Communities
Taxonomic Characterization of Closed Microbial Communities
Metabolic Characterization of Closed Microbial Communities
Discussion
Findings
Materials and Methods
Full Text
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