Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership

ABSTRACT The mechanisms by which microbes interact in communities remain poorly understood. Here, we interrogated specific interactions between photoautotrophic and heterotrophic members of a model consortium to infer mechanisms that mediate metabolic coupling and acclimation to partnership. This bi...

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Autores principales:	Hans C. Bernstein, Ryan S. McClure, Vera Thiel, Natalie C. Sadler, Young-Mo Kim, William B. Chrisler, Eric A. Hill, Donald A. Bryant, Margaret F. Romine, Janet K. Jansson, Jim K. Fredrickson, Alexander S. Beliaev
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	consortia cyanobacteria heterotroph microbial interactions transcriptome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dbe4c1fd29e745e0ba277ae1c1675927
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spelling	oai:doaj.org-article:dbe4c1fd29e745e0ba277ae1c16759272021-12-02T18:39:34ZIndirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership10.1128/mSystems.00181-162379-5077https://doaj.org/article/dbe4c1fd29e745e0ba277ae1c16759272017-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00181-16https://doaj.org/toc/2379-5077ABSTRACT The mechanisms by which microbes interact in communities remain poorly understood. Here, we interrogated specific interactions between photoautotrophic and heterotrophic members of a model consortium to infer mechanisms that mediate metabolic coupling and acclimation to partnership. This binary consortium was composed of a cyanobacterium, Thermosynechococcus elongatus BP-1, which supported growth of an obligate aerobic heterotroph, Meiothermus ruber strain A, by providing organic carbon, O2, and reduced nitrogen. Species-resolved transcriptomic analyses were used in combination with growth and photosynthesis kinetics to infer interactions and the environmental context under which they occur. We found that the efficiency of biomass production and resistance to stress induced by high levels of dissolved O2 increased, beyond axenic performance, as a result of heterotrophic partnership. Coordinated transcriptional responses transcending both species were observed and used to infer specific interactions resulting from the synthesis and exchange of resources. The cyanobacterium responded to heterotrophic partnership by altering expression of core genes involved with photosynthesis, carbon uptake/fixation, vitamin synthesis, and scavenging of reactive oxygen species (ROS). IMPORTANCE This study elucidates how a cyanobacterial primary producer acclimates to heterotrophic partnership by modulating the expression levels of key metabolic genes. Heterotrophic bacteria can indirectly regulate the physiology of the photoautotrophic primary producers, resulting in physiological changes identified here, such as increased intracellular ROS. Some of the interactions inferred from this model system represent putative principles of metabolic coupling in phototrophic-heterotrophic partnerships.Hans C. BernsteinRyan S. McClureVera ThielNatalie C. SadlerYoung-Mo KimWilliam B. ChrislerEric A. HillDonald A. BryantMargaret F. RomineJanet K. JanssonJim K. FredricksonAlexander S. BeliaevAmerican Society for Microbiologyarticleconsortiacyanobacteriaheterotrophmicrobial interactionstranscriptomeMicrobiologyQR1-502ENmSystems, Vol 2, Iss 2 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	consortia cyanobacteria heterotroph microbial interactions transcriptome Microbiology QR1-502
spellingShingle	consortia cyanobacteria heterotroph microbial interactions transcriptome Microbiology QR1-502 Hans C. Bernstein Ryan S. McClure Vera Thiel Natalie C. Sadler Young-Mo Kim William B. Chrisler Eric A. Hill Donald A. Bryant Margaret F. Romine Janet K. Jansson Jim K. Fredrickson Alexander S. Beliaev Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership
description	ABSTRACT The mechanisms by which microbes interact in communities remain poorly understood. Here, we interrogated specific interactions between photoautotrophic and heterotrophic members of a model consortium to infer mechanisms that mediate metabolic coupling and acclimation to partnership. This binary consortium was composed of a cyanobacterium, Thermosynechococcus elongatus BP-1, which supported growth of an obligate aerobic heterotroph, Meiothermus ruber strain A, by providing organic carbon, O2, and reduced nitrogen. Species-resolved transcriptomic analyses were used in combination with growth and photosynthesis kinetics to infer interactions and the environmental context under which they occur. We found that the efficiency of biomass production and resistance to stress induced by high levels of dissolved O2 increased, beyond axenic performance, as a result of heterotrophic partnership. Coordinated transcriptional responses transcending both species were observed and used to infer specific interactions resulting from the synthesis and exchange of resources. The cyanobacterium responded to heterotrophic partnership by altering expression of core genes involved with photosynthesis, carbon uptake/fixation, vitamin synthesis, and scavenging of reactive oxygen species (ROS). IMPORTANCE This study elucidates how a cyanobacterial primary producer acclimates to heterotrophic partnership by modulating the expression levels of key metabolic genes. Heterotrophic bacteria can indirectly regulate the physiology of the photoautotrophic primary producers, resulting in physiological changes identified here, such as increased intracellular ROS. Some of the interactions inferred from this model system represent putative principles of metabolic coupling in phototrophic-heterotrophic partnerships.
format	article
author	Hans C. Bernstein Ryan S. McClure Vera Thiel Natalie C. Sadler Young-Mo Kim William B. Chrisler Eric A. Hill Donald A. Bryant Margaret F. Romine Janet K. Jansson Jim K. Fredrickson Alexander S. Beliaev
author_facet	Hans C. Bernstein Ryan S. McClure Vera Thiel Natalie C. Sadler Young-Mo Kim William B. Chrisler Eric A. Hill Donald A. Bryant Margaret F. Romine Janet K. Jansson Jim K. Fredrickson Alexander S. Beliaev
author_sort	Hans C. Bernstein
title	Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership
title_short	Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership
title_full	Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership
title_fullStr	Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership
title_full_unstemmed	Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership
title_sort	indirect interspecies regulation: transcriptional and physiological responses of a cyanobacterium to heterotrophic partnership
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/dbe4c1fd29e745e0ba277ae1c1675927
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Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership

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