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The contrasting roles of nitric oxide drive microbial community organization as a function of oxygen presence

Wilbert, Steven A. and Newman, Dianne K. (2022) The contrasting roles of nitric oxide drive microbial community organization as a function of oxygen presence. Current Biology, 32 (24). 5221-5234.e4. ISSN 0960-9822. PMCID PMC9772256. doi:10.1016/j.cub.2022.10.008.

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Microbial assemblages are omnipresent in the biosphere, forming communities on the surfaces of roots and rocks and within living tissues. These communities can exhibit strikingly beautiful compositional structures, with certain members reproducibly occupying particular spatiotemporal microniches. Despite this reproducibility, we lack the ability to explain these spatial patterns. We hypothesize that certain spatial patterns in microbial communities may be explained by the exchange of redox-active metabolites whose biological function is sensitive to microenvironmental gradients. To test this, 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 and fitness outcomes in a predictable fashion. Using a combination of genetic analysis, controlled growth environments, and imaging, we show that oxygen availability dictates whether NO cross-feeding is deleterious or mutually beneficial and that this organizing principle maps to the microscale. More generally, this work underscores the importance of considering the double-edged and microenvironmentally tuned roles redox-active metabolites can play in shaping microbial communities.

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Newman, Dianne K.0000-0003-1647-1918
Additional Information: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 manuscript review; Dr. Melanie Spero for molecular technique instruction; Drs. Reinaldo Alcade, Georgia Squyres, Zachary Lonergan for fruitful discussion and assay troubleshooting; and Dr. Michael Piacentino for help with programming and encouragement. Some of the imaging was performed in the Biological Imaging Facility of the California Institute of Technology with the support of the Caltech Beckman Institute and the Arnold and Mabel Beckman Foundation.
Group:Division of Geological and Planetary Sciences
Funding AgencyGrant Number
NSF Graduate Research FellowshipUNSPECIFIED
Caltech Beckman InstituteUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
Issue or Number:24
PubMed Central ID:PMC9772256
Record Number:CaltechAUTHORS:20230203-893210800.2
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:119002
Deposited By: Research Services Depository
Deposited On:24 Feb 2023 19:56
Last Modified:23 Mar 2023 21:02

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