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

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 w...

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Autores principales:	Kyle C. Costa, Megan Bergkessel, Scott Saunders, Jonas Korlach, Dianne K. Newman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/18f5c51862ea41a1938c11359e1eb2d4
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spelling	oai:doaj.org-article:18f5c51862ea41a1938c11359e1eb2d42021-11-15T15:41:24ZEnzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity10.1128/mBio.01520-152150-7511https://doaj.org/article/18f5c51862ea41a1938c11359e1eb2d42015-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01520-15https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Phenazine production by Pseudomonas spp. can shape microbial communities in a variety of environments ranging from the cystic fibrosis lung to the rhizosphere of dryland crops. For example, in the rhizosphere, phenazines can protect plants from infection by pathogenic fungi. The redox activity of phenazines underpins their antibiotic activity, as well as providing pseudomonads with important physiological benefits. Our discovery that soil mycobacteria can catabolize phenazines and thereby protect other organisms against phenazine toxicity suggests that phenazine degradation may influence turnover in situ. The identification of genes involved in the degradation of phenazines opens the door to monitoring turnover in diverse environments, an essential process to consider when one is attempting to understand or control communities influenced by phenazines.Kyle C. CostaMegan BergkesselScott SaundersJonas KorlachDianne K. NewmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 6 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Kyle C. Costa Megan Bergkessel Scott Saunders Jonas Korlach Dianne K. Newman Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity
description	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. IMPORTANCE Phenazine production by Pseudomonas spp. can shape microbial communities in a variety of environments ranging from the cystic fibrosis lung to the rhizosphere of dryland crops. For example, in the rhizosphere, phenazines can protect plants from infection by pathogenic fungi. The redox activity of phenazines underpins their antibiotic activity, as well as providing pseudomonads with important physiological benefits. Our discovery that soil mycobacteria can catabolize phenazines and thereby protect other organisms against phenazine toxicity suggests that phenazine degradation may influence turnover in situ. The identification of genes involved in the degradation of phenazines opens the door to monitoring turnover in diverse environments, an essential process to consider when one is attempting to understand or control communities influenced by phenazines.
format	article
author	Kyle C. Costa Megan Bergkessel Scott Saunders Jonas Korlach Dianne K. Newman
author_facet	Kyle C. Costa Megan Bergkessel Scott Saunders Jonas Korlach Dianne K. Newman
author_sort	Kyle C. Costa
title	Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity
title_short	Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity
title_full	Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity
title_fullStr	Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity
title_full_unstemmed	Enzymatic Degradation of Phenazines Can Generate Energy and Protect Sensitive Organisms from Toxicity
title_sort	enzymatic degradation of phenazines can generate energy and protect sensitive organisms from toxicity
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/18f5c51862ea41a1938c11359e1eb2d4
work_keys_str_mv	AT kyleccosta enzymaticdegradationofphenazinescangenerateenergyandprotectsensitiveorganismsfromtoxicity AT meganbergkessel enzymaticdegradationofphenazinescangenerateenergyandprotectsensitiveorganismsfromtoxicity AT scottsaunders enzymaticdegradationofphenazinescangenerateenergyandprotectsensitiveorganismsfromtoxicity AT jonaskorlach enzymaticdegradationofphenazinescangenerateenergyandprotectsensitiveorganismsfromtoxicity AT dianneknewman enzymaticdegradationofphenazinescangenerateenergyandprotectsensitiveorganismsfromtoxicity
_version_	1718427690332061696

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

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