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Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity

Costa, Kyle C. and Bergkessel, Megan and Saunders, Scott and Korlach, Jonas and Newman, Dianne K. (2015) Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity. mBio, 6 (6). Art. No. e01520-15. ISSN 2150-7511. PMCID PMC4626857. http://resolver.caltech.edu/CaltechAUTHORS:20151102-105401926

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Abstract

Diverse bacteria, including several Pseudomonas species, produce a class of redox-active metabolites called phenazines that impact different cell types in nature and disease. Phenazines can affect microbial communities in both positive and negative ways, where their presence is correlated with decreased species richness and diversity. However, little is known about how the concentration of phenazines is modulated in situ and what this may mean for the fitness of members of the community. Through culturing of phenazine-degrading mycobacteria, genome sequencing, comparative genomics, and molecular analysis, we identified several conserved genes that are important for the degradation of three Pseudomonas-derived phenazines: phenazine-1-carboxylic acid (PCA), phenazine-1-carboxamide (PCN), and pyocyanin (PYO). PCA can be used as the sole carbon source for growth by these organisms. Deletion of several genes in Mycobacterium fortuitum abolishes the degradation phenotype, and expression of two genes in a heterologous host confers the ability to degrade PCN and PYO. In cocultures with phenazine producers, phenazine degraders alter the abundance of different phenazine types. Not only does degradation support mycobacterial catabolism, but also it provides protection to bacteria that would otherwise be inhibited by the toxicity of PYO. Collectively, these results serve as a reminder that microbial metabolites can be actively modified and degraded and that these turnover processes must be considered when the fate and impact of such compounds in any environment are being assessed.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1128/mBio.01520-15DOIArticle
http://mbio.asm.org/content/6/6/e01520-15PublisherArticle
http://mbio.asm.org/lookup/suppl/doi:10.1128/mBio.01520-15/-/DCSupplementalPublisherSupplementary Data
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4626857/PubMed CentralArticle
ORCID:
AuthorORCID
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2015 Costa et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Received 7 September 2015; Accepted 5 October 2015; Published 27 October 2015. We thank Jon Van Hamme and Lindsay Eltis for providing Rhodococcus strains JVH1 and RHA1. We also thank members of the Newman lab for helpful feedback. K.C.C. was supported by a Ruth L. Kirschstein National Research Service Award F32 from the NIH, award no. F32AI112248. This work was further supported by the Howard Hughes Medical Institute (HHMI) and the Millard and Muriel Genetics and Genomics Laboratory at the California Institute of Technology; D.K.N. is an HHMI investigator.
Funders:
Funding AgencyGrant Number
NIHF32AI112248
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Caltech Millard and Muriel Jacobs Genetics and Genomics LaboratoryUNSPECIFIED
PubMed Central ID:PMC4626857
Record Number:CaltechAUTHORS:20151102-105401926
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20151102-105401926
Official Citation:Costa KC, Bergkessel M, Saunders S, Korlach J, Newman DK. 2015. Enzymatic degradation of phenazines can generate energy and protect sensitive organisms from toxicity. mBio 6(6):e01520-15. doi:10.1128/mBio.01520-15.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:61769
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:02 Nov 2015 20:49
Last Modified:17 May 2018 21:17

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