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Title: Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis

Abstract

Dinitrogen (N2)-fixation by cyanobacteria in symbiosis with feather mosses represents the main pathway of biological N input into boreal forests. Despite its significance, little is known about the gene repertoire needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions or regulatory rewiring allowing cyanobacteria to form this symbiosis, we compared closely related Nostoc strains that were either symbiosis-competent or non-competent, using a proteogenomics approach and a unique experimental setup allowing for controlled chemical and physical contact between partners. Thirty-two protein families were only in the genomes of competent strains, including some never before associated with symbiosis. We identified conserved orthologs that were differentially expressed in competent strains, including gene families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, sugar metabolism, and glycosyl-modifying and oxidative stress-mediating exoenzymes. In contrast to other cyanobacteria-plant symbioses, the moss-cyanobacteria epiphytic symbiosis is distinct, with the symbiont retaining motility and chemotaxis, and not modulating N-fixation, photosynthesis, GS-GOGAT cycle, and heterocyst formation. Our work expands our knowledge of plant cyanobacterial symbioses, provides an interaction model of this ecologically significant symbiosis, and suggests new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintaining this symbiosis.

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1422344
Report Number(s):
PNNL-SA-127738
Journal ID: ISSN 1751-7370; 48081; KP1704020
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: The ISME Journal; Journal Volume: 11; Journal Issue: 12; Related Information: 2821–2833
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Warshan, Denis, Espinoza, Josh L., Stuart, Rhona, Richter, Alexander R., Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, Kyripides, Nikos, Barry, Kerrie W., Singan, Vasanth, Lindquist, Erika, Ansong, Charles K., Purvine, Samuel O., Brewer, Heather M., Weyman, Philip D., Dupont, Chris, and Rasmussen, Ulla. Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis. United States: N. p., 2017. Web. doi:10.1038/ismej.2017.134.
Warshan, Denis, Espinoza, Josh L., Stuart, Rhona, Richter, Alexander R., Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, Kyripides, Nikos, Barry, Kerrie W., Singan, Vasanth, Lindquist, Erika, Ansong, Charles K., Purvine, Samuel O., Brewer, Heather M., Weyman, Philip D., Dupont, Chris, & Rasmussen, Ulla. Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis. United States. doi:10.1038/ismej.2017.134.
Warshan, Denis, Espinoza, Josh L., Stuart, Rhona, Richter, Alexander R., Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, Kyripides, Nikos, Barry, Kerrie W., Singan, Vasanth, Lindquist, Erika, Ansong, Charles K., Purvine, Samuel O., Brewer, Heather M., Weyman, Philip D., Dupont, Chris, and Rasmussen, Ulla. Sun . "Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis". United States. doi:10.1038/ismej.2017.134.
@article{osti_1422344,
title = {Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis},
author = {Warshan, Denis and Espinoza, Josh L. and Stuart, Rhona and Richter, Alexander R. and Kim, Sea-Yong and Shapiro, Nicole and Woyke, Tanja and Kyripides, Nikos and Barry, Kerrie W. and Singan, Vasanth and Lindquist, Erika and Ansong, Charles K. and Purvine, Samuel O. and Brewer, Heather M. and Weyman, Philip D. and Dupont, Chris and Rasmussen, Ulla},
abstractNote = {Dinitrogen (N2)-fixation by cyanobacteria in symbiosis with feather mosses represents the main pathway of biological N input into boreal forests. Despite its significance, little is known about the gene repertoire needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions or regulatory rewiring allowing cyanobacteria to form this symbiosis, we compared closely related Nostoc strains that were either symbiosis-competent or non-competent, using a proteogenomics approach and a unique experimental setup allowing for controlled chemical and physical contact between partners. Thirty-two protein families were only in the genomes of competent strains, including some never before associated with symbiosis. We identified conserved orthologs that were differentially expressed in competent strains, including gene families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, sugar metabolism, and glycosyl-modifying and oxidative stress-mediating exoenzymes. In contrast to other cyanobacteria-plant symbioses, the moss-cyanobacteria epiphytic symbiosis is distinct, with the symbiont retaining motility and chemotaxis, and not modulating N-fixation, photosynthesis, GS-GOGAT cycle, and heterocyst formation. Our work expands our knowledge of plant cyanobacterial symbioses, provides an interaction model of this ecologically significant symbiosis, and suggests new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintaining this symbiosis.},
doi = {10.1038/ismej.2017.134},
journal = {The ISME Journal},
number = 12,
volume = 11,
place = {United States},
year = {Sun Dec 31 00:00:00 EST 2017},
month = {Sun Dec 31 00:00:00 EST 2017}
}