title: 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 binary consortium was composed of a cyanobacterium,Thermosynechococcus elongatusBP-1, which supported growth of an obligate aerobic heterotroph,Meiothermus ruberstrain 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 O2increased, 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).IMPORTANCEThis 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.
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA; The Gene and Linda Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington, USA.
authors.forename: Hans C
authors.identifier: 0000-0003-2913-7708
authors.initials: HC
authors.lastname: Bernstein
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Ryan S
authors.initials: RS
authors.lastname: McClure
authors.affiliation: Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania, USA.
authors.forename: Vera
authors.initials: V
authors.lastname: Thiel
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Natalie C
authors.initials: NC
authors.lastname: Sadler
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Young-Mo
authors.initials: YM
authors.lastname: Kim
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA; Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: William B
authors.initials: WB
authors.lastname: Chrisler
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Eric A
authors.initials: EA
authors.lastname: Hill
authors.affiliation: Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania, USA; Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana, USA.
authors.forename: Donald A
authors.identifier: 0000-0003-2782-5988
authors.initials: DA
authors.lastname: Bryant
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Margaret F
authors.initials: MF
authors.lastname: Romine
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Janet K
authors.initials: JK
authors.lastname: Jansson
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Jim K
authors.initials: JK
authors.lastname: Fredrickson
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.
authors.forename: Alexander S
authors.initials: AS
authors.lastname: Beliaev
keywords: consortia; cyanobacteria; heterotroph; microbial interactions; transcriptome