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The double-edged role of nitric oxide drives predictable microbial community organization according to the microenvironment

Wilbert, Steven A. and Newman, Dianne K. (2021) The double-edged role of nitric oxide drives predictable microbial community organization according to the microenvironment. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20211210-238484000

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Abstract

Microbial assemblages are omnipresent in the biosphere, forming communities on the surfaces of roots, rocks, and within living tissues. These communities can exhibit strikingly beautiful compositional structures, with certain members reproducibly occupying particular spatiotemporal microniches. Yet often, we lack the ability to explain the spatial patterns we see within them. To test the hypothesis that certain spatial patterns in microbial communities may be explained by the exchange of redox-active metabolites whose biological function is sensitive to environmental gradients, here we developed a simple community consisting of synthetic Pseudomonas aeruginosa strains with a partitioned denitrification pathway: a strict consumer and strict producer of nitric oxide (NO), a key pathway intermediate. Because NO can be both toxic or beneficial depending on the amount of oxygen present, this system provided an opportunity to investigate whether dynamic oxygen gradients can tune metabolic cross-feeding in a predictable fashion. Using a combination of genetic analysis, different growth environments and imaging, we show that oxygen availability controls whether NO cross-feeding is commensal or mutually beneficial, and that this organizing principle maps to the microscale. More generally, this work underscores the importance of considering the double-edged roles redox-active metabolites can play in shaping microbial communities.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.12.09.472001DOIDiscussion Paper
ORCID:
AuthorORCID
Newman, Dianne K.0000-0003-1647-1918
Additional Information: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. The work was supported by the National Institutes of Health (R01HL152190 to D.K.N.) and the National Science Foundation Graduate Student Fellowships Program (to S.A.W.). We would like to thank the current and past Newman Lab members for feedback and discussions. Specifically, we thank Drs. Darcy McRose and Avi Flamholz for critical manuscript review, Dr. Melanie Spero for molecular technique instruction, Drs. Reinaldo Alcade and Georgia Squyres for fruitful discussion and troubleshooting imaging assays, and Dr. Michael Piacentino for help with coding and general morale. The authors have declared no competing interest.
Funders:
Funding AgencyGrant Number
NIHR01HL152190
NSF Graduate Research FellowshipUNSPECIFIED
Subject Keywords:Polymicrobial communities, metabolism, metabolic cross-feeding, nitric oxide, nitrate, denitrification, spatial organization, microenvironment, oxygen gradients, Pseudomonas aeruginosa
DOI:10.1101/2021.12.09.472001
Record Number:CaltechAUTHORS:20211210-238484000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211210-238484000
Official Citation:The double-edged role of nitric oxide drives predictable microbial community organization according to the microenvironment Steven A. Wilbert, Dianne K. Newman bioRxiv 2021.12.09.472001; doi: https://doi.org/10.1101/2021.12.09.472001
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112354
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:10 Dec 2021 22:35
Last Modified:10 Dec 2021 22:35

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