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

Bernstein, Hans C.; McClure, Ryan S.; Thiel, Vera; Sadler, Natalie C.; Kim, Young-Mo; Chrisler, William B.; Hill, Eric A.; Bryant, Donald A.; Romine, Margaret F.; Jansson, Janet K.; Fredrickson, Jim K.; Beliaev, Alexander S.

doi:10.1128/msystems.00181-16

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

Journal Article · 07 March 2017 · mSystems

DOI: https://doi.org/10.1128/msystems.00181-16 · OSTI ID:1626177

^[1]; McClure, Ryan S. ^[2]; Thiel, Vera ^[3]; Sadler, Natalie C. ^[2]; Kim, Young-Mo ^[2]; Chrisler, William B. ^[4]; Hill, Eric A. ^[2];

^[5]; Romine, Margaret F. ^[2]; Jansson, Janet K. ^[2]; Fredrickson, Jim K. ^[2]; Beliaev, Alexander S. ^[2]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Washington State Univ., Pullman, WA (United States); DOE/OSTI
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Pennsylvania State Univ., University Park, PA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
Pennsylvania State Univ., University Park, PA (United States); Montana State Univ., Bozeman, MT (United States)

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. 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 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). 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.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC06-76RL01830

OSTI ID:: 1626177

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 2 Vol. 2; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Feedback-controlled LED photobioreactor for photophysiological studies of cyanobacteria Melnicki, Matthew R.; Pinchuk, Grigoriy E.; Hill, Eric A. Bioresource Technology, Vol. 134 https://doi.org/10.1016/j.biortech.2013.01.079	journal	April 2013
Direct measurement and characterization of active photosynthesis zones inside wastewater remediating and biofuel producing microalgal biofilms Bernstein, Hans C.; Kesaano, Maureen; Moll, Karen Bioresource Technology, Vol. 156 https://doi.org/10.1016/j.biortech.2014.01.001	journal	March 2014
Synthetic Escherichia coli consortia engineered for syntrophy demonstrate enhanced biomass productivity Bernstein, Hans C.; Paulson, Steven D.; Carlson, Ross P. Journal of Biotechnology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jbiotec.2011.10.001	journal	January 2012
Functional and Structural Characterization of the 2/2 Hemoglobin from Synechococcus sp. PCC 7002, Scott, Nancy L.; Xu, Yu; Shen, Gaozhong Biochemistry, Vol. 49, Issue 33 https://doi.org/10.1021/bi100463d	journal	August 2010
Inference of interactions in cyanobacterial–heterotrophic co-cultures via transcriptome sequencing Beliaev, Alexander S.; Romine, Margie F.; Serres, Margrethe The ISME Journal, Vol. 8, Issue 11 https://doi.org/10.1038/ismej.2014.69	journal	April 2014
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Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals Aharonovich, Dikla; Sher, Daniel The ISME Journal, Vol. 10, Issue 12 https://doi.org/10.1038/ismej.2016.70	journal	April 2016
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Circadian Rhythms in the Thermophilic Cyanobacterium Thermosynechococcus elongatus: Compensation of Period Length over a Wide Temperature Range Onai, Kiyoshi; Morishita, Megumi; Itoh, Shino Journal of Bacteriology, Vol. 186, Issue 15 https://doi.org/10.1128/JB.186.15.4972-4977.2004	journal	August 2004
Draft Genome Sequence of the Deinococcus-Thermus Bacterium Meiothermus ruber Strain A Thiel, Vera; Tomsho, Lynn P.; Burhans, Richard Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomeA.00202-15	journal	March 2015
Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth Bernstein, Hans C.; McClure, Ryan S.; Hill, Eric A. mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.00949-16	journal	July 2016
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Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean's Surface Morris, J. Jeffrey; Johnson, Zackary I.; Szul, Martin J. PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016805	journal	February 2011
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Effect of mono- and dichromatic light quality on growth rates and photosynthetic performance of Synechococcus sp. PCC 7002 Bernstein, Hans C.; Konopka, Allan; Melnicki, Matthew R. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00488	journal	September 2014
The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light Nowack, Shane; Olsen, Millie T.; Schaible, George A. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00626	journal	June 2015
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Microbial Consortia Engineering for Cellular Factories: in Vitro to in Silico Systems Bernstein, Hans C.; Carlson, Ross P. Computational and Structural Biotechnology Journal, Vol. 3, Issue 4 https://doi.org/10.5936/csbj.201210017	journal	October 2012

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Additional file 4 of Construction and analysis of an artificial consortium based on the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 to produce the platform chemical 3-hydroxypropionic acid from CO2 Zhang, Li; Chen, Lei; Diao, Jinjin figshare https://doi.org/10.6084/m9.figshare.12262847.v1	image	January 2020
Additional file 6 of Construction and analysis of an artificial consortium based on the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 to produce the platform chemical 3-hydroxypropionic acid from CO2 Zhang, Li; Chen, Lei; Diao, Jinjin figshare https://doi.org/10.6084/m9.figshare.12262859.v1	image	January 2020
Additional file 7 of Construction and analysis of an artificial consortium based on the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 to produce the platform chemical 3-hydroxypropionic acid from CO2 Zhang, Li; Chen, Lei; Diao, Jinjin figshare https://doi.org/10.6084/m9.figshare.12262862.v1	image	January 2020
Additional file 2 of Cross-feeding between cyanobacterium Synechococcus and Escherichia coli in an artificial autotrophic–heterotrophic coculture system revealed by integrated omics analysis Ma, Jiajia; Guo, Taohong; Ren, Meijin figshare https://doi.org/10.6084/m9.figshare.20131174.v1	image	January 2022
Additional file 3 of Cross-feeding between cyanobacterium Synechococcus and Escherichia coli in an artificial autotrophic–heterotrophic coculture system revealed by integrated omics analysis Ma, Jiajia; Guo, Taohong; Ren, Meijin figshare https://doi.org/10.6084/m9.figshare.20131177.v1	image	January 2022
Additional file 4 of Cross-feeding between cyanobacterium Synechococcus and Escherichia coli in an artificial autotrophic–heterotrophic coculture system revealed by integrated omics analysis Ma, Jiajia; Guo, Taohong; Ren, Meijin figshare https://doi.org/10.6084/m9.figshare.20131180	image	January 2022
Additional file 5 of Cross-feeding between cyanobacterium Synechococcus and Escherichia coli in an artificial autotrophic–heterotrophic coculture system revealed by integrated omics analysis Ma, Jiajia; Guo, Taohong; Ren, Meijin figshare https://doi.org/10.6084/m9.figshare.20131183	image	January 2022
Additional file 6 of Cross-feeding between cyanobacterium Synechococcus and Escherichia coli in an artificial autotrophic–heterotrophic coculture system revealed by integrated omics analysis Ma, Jiajia; Guo, Taohong; Ren, Meijin figshare https://doi.org/10.6084/m9.figshare.20131186.v1	image	January 2022
Species-specific transcriptomic network inference of interspecies interactions McClure, Ryan S.; Overall, Christopher C.; Hill, Eric A. The ISME Journal, Vol. 12, Issue 8 https://doi.org/10.1038/s41396-018-0145-6	journal	May 2018
Phenotypic responses to interspecies competition and commensalism in a naturally-derived microbial co-culture Khan, Nymul; Maezato, Yukari; McClure, Ryan S. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-18630-1	journal	January 2018
Heterotroph Interactions Alter Prochlorococcus Transcriptome Dynamics during Extended Periods of Darkness Biller, Steven J.; Coe, Allison; Roggensack, Sara E. mSystems, Vol. 3, Issue 3 https://doi.org/10.1128/msystems.00040-18	journal	May 2018
Construction and analysis of an artificial consortium based on the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 to produce the platform chemical 3-hydroxypropionic acid from CO2 Zhang, Li; Chen, Lei; Diao, Jinjin Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01720-0	journal	May 2020
Effect of light wavelength on hot spring microbial mat biodiversity Nishida, Akifumi; Thiel, Vera; Nakagawa, Mayuko PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0191650	journal	January 2018
The Ecology of Subaerial Biofilms in Dry and Inhospitable Terrestrial Environments Villa, Federica; Cappitelli, Francesca Microorganisms, Vol. 7, Issue 10 https://doi.org/10.3390/microorganisms7100380	journal	September 2019

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