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Ecological stochasticity and phage induction diversify bacterioplankton communities at the microscale

View ORCID ProfileRachel E. Szabo, View ORCID ProfileSammy Pontrelli, View ORCID ProfileJacopo Grilli, View ORCID ProfileJulia A. Schwartzman, View ORCID ProfileShaul Pollak, View ORCID ProfileUwe Sauer, View ORCID ProfileOtto X. Cordero
doi: https://doi.org/10.1101/2021.09.27.461956
Rachel E. Szabo
aMicrobiology Graduate Program, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
bDepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Sammy Pontrelli
cInstitute of Molecular Systems Biology, ETH Zürich, 8093 Zürich, Switzerland.
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Jacopo Grilli
dQuantitative Life Sciences, The Abdus Salam International Centre for Theoretical Physics, 34151 Trieste, Italy.
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Julia A. Schwartzman
bDepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Shaul Pollak
bDepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Uwe Sauer
cInstitute of Molecular Systems Biology, ETH Zürich, 8093 Zürich, Switzerland.
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Otto X. Cordero
bDepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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  • For correspondence: ottox@mit.edu
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Abstract

In many natural environments, microorganisms self-assemble around heterogeneously distributed resource patches. The growth and collapse of populations on resource patches can unfold within spatial ranges of a few hundred micrometers or less, making such microscale ecosystems hotspots of biological interactions and nutrient fluxes. Despite the potential importance of patch-level dynamics for the large-scale evolution and function of microbial communities, we have not yet been able to delineate the ecological processes that control natural populations at the microscale. Here, we addressed this challenge in the context of microbially-mediated degradation of particulate organic matter by characterizing the natural marine communities that assembled on over one thousand individual microscale chitin particles. Through shotgun metagenomics, we found significant variation in microscale community composition despite the similarity in initial species pools across replicates. Strikingly, a subset of particles was highly populated by rare chitin-degrading strains; we hypothesized that their conditional success reflected the impact of stochastic colonization and growth on community assembly. In contrast to the conserved functional structures that emerge in ecosystems at larger scales, this taxonomic variability translated to a wide range of predicted chitinolytic abilities and growth returns at the level of individual particles. We found that predation by temperate bacteriophages, especially of degrader strains, was a significant contributor to the variability in the bacterial compositions and yields observed across communities. Our study suggests that initial stochasticity in assembly states at the microscale, amplified through biotic interactions, may have significant consequences for the diversity and functionality of microbial communities at larger scales.

Significance Statement The biogeochemical consequences of the degradation of particulate organic matter by microorganisms represent the cumulative effect of microbial activity on individual microscale resource patches. The ecological processes controlling community dynamics in these highly localized microenvironments remain poorly understood. Here, we find that complex marine communities growing on microscale resource particles diverge both taxonomically and functionally despite assembling under identical abiotic conditions from a common species pool. We show that this variability stems from bacteriophage predation and history-dependent factors in community assembly, which create stochastic dynamics that are spatially structured at the microscale. This microscale stochasticity may have significant consequences for the coexistence, evolution, and function of diverse bacterial and viral populations in the global ocean.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing Interest Statement: The authors declare no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 27, 2021.
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Ecological stochasticity and phage induction diversify bacterioplankton communities at the microscale
Rachel E. Szabo, Sammy Pontrelli, Jacopo Grilli, Julia A. Schwartzman, Shaul Pollak, Uwe Sauer, Otto X. Cordero
bioRxiv 2021.09.27.461956; doi: https://doi.org/10.1101/2021.09.27.461956
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Ecological stochasticity and phage induction diversify bacterioplankton communities at the microscale
Rachel E. Szabo, Sammy Pontrelli, Jacopo Grilli, Julia A. Schwartzman, Shaul Pollak, Uwe Sauer, Otto X. Cordero
bioRxiv 2021.09.27.461956; doi: https://doi.org/10.1101/2021.09.27.461956

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