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

Abstract

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, O 2, 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 O 2 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 ofmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [2];  [2];  [4];  [2]; ORCiD logo [5];  [2];  [2];  [2];  [2]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Washington State Univ., Pullman, WA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Pennsylvania State Univ., University Park, PA (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
  5. Pennsylvania State Univ., University Park, PA (United States); Montana State Univ., Bozeman, MT (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1626177
Grant/Contract Number:  
AC06-76RL01830; 49356
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 2; Journal Issue: 2; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; consortia; cyanobacteria; heterotroph; microbial interactions; transcriptome

Citation Formats

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., and Beliaev, Alexander S. Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership. United States: N. p., 2017. Web. doi:10.1128/msystems.00181-16.
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. Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership. United States. doi:10.1128/msystems.00181-16.
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., and Beliaev, Alexander S. Tue . "Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership". United States. doi:10.1128/msystems.00181-16. https://www.osti.gov/servlets/purl/1626177.
@article{osti_1626177,
title = {Indirect Interspecies Regulation: Transcriptional and Physiological Responses of a Cyanobacterium to Heterotrophic Partnership},
author = {Bernstein, Hans C. and McClure, Ryan S. and Thiel, Vera and Sadler, Natalie C. and Kim, Young-Mo and Chrisler, William B. and Hill, Eric A. and Bryant, Donald A. and Romine, Margaret F. and Jansson, Janet K. and Fredrickson, Jim K. and Beliaev, Alexander S.},
abstractNote = {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.},
doi = {10.1128/msystems.00181-16},
journal = {mSystems},
issn = {2379-5077},
number = 2,
volume = 2,
place = {United States},
year = {2017},
month = {3}
}

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