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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 feathermosses is the primary pathway of biological nitrogen (N) input into boreal forests. Despite its significance, little is known about the cyanobacterial gene repertoire and regulatory rewiring needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions and regulatory changes allowing cyanobacteria to form and maintain this symbiosis, we compared genomically closely related symbiotic-competent and -incompetent Nostoc strains using a proteogenomics approach and an experimental set up allowing for controlled chemical and physical contact between partners. Thirty-two gene families were found only in the genomes of symbiotic strains, including some never before associated with cyanobacterial symbiosis. We identified conserved orthologs that were differentially expressed in symbiotic strains, including protein families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, and glycosyl-modifying and oxidative stress-mediating exoenzymes. The physical moss–cyanobacteria epiphytic symbiosis is distinct from other cyanobacteria–plant symbioses, with Nostoc retaining motility, and lacking modulation of N2-fixation, photosynthesis, GS-GOGAT cycle and heterocyst formation. The results expand our knowledge base of plant–cyanobacterial symbioses, provide a model of information and material exchange in this ecologically significant symbiosis, and suggest new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintainingmore » the cyanobacteria–feathermoss symbiosis.« less

Authors:
 [1];  [2];  [3];  [2];  [1];  [4];  [4];  [4];  [4]; ORCiD logo [4];  [4];  [5];  [6]; ORCiD logo [6];  [2];  [2];  [1]
  1. Stockholm Univ. (Sweden). Department of Ecology, Environment and Plant Sciences
  2. J Craig Venter Institute, La Jolla, CA (United States)
  3. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
  6. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1409934
Alternate Identifier(s):
OSTI ID: 1430726
Report Number(s):
LLNL-JRNL-730832; PNNL-SA-127738
Journal ID: ISSN 1751-7362
Grant/Contract Number:  
AC52-07NA27344; AC02-05CH11231; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 11; Journal Issue: 12; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Boreal forest; Comparative genomic; Transcriptomic; Proteomic; Exoproteomic

Citation Formats

Warshan, Denis, Espinoza, Josh L., Stuart, Rhona K., Richter, R. Alexander, Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, C. Kyrpides, Nikos, Barry, Kerrie, Singan, Vasanth, Lindquist, Erika, Ansong, Charles, Purvine, Samuel O., M. Brewer, Heather, Weyman, Philip D., Dupont, Christopher L., 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 K., Richter, R. Alexander, Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, C. Kyrpides, Nikos, Barry, Kerrie, Singan, Vasanth, Lindquist, Erika, Ansong, Charles, Purvine, Samuel O., M. Brewer, Heather, Weyman, Philip D., Dupont, Christopher L., & 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 K., Richter, R. Alexander, Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, C. Kyrpides, Nikos, Barry, Kerrie, Singan, Vasanth, Lindquist, Erika, Ansong, Charles, Purvine, Samuel O., M. Brewer, Heather, Weyman, Philip D., Dupont, Christopher L., and Rasmussen, Ulla. Fri . "Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis". United States. doi:10.1038/ismej.2017.134. https://www.osti.gov/servlets/purl/1409934.
@article{osti_1409934,
title = {Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis},
author = {Warshan, Denis and Espinoza, Josh L. and Stuart, Rhona K. and Richter, R. Alexander and Kim, Sea-Yong and Shapiro, Nicole and Woyke, Tanja and C. Kyrpides, Nikos and Barry, Kerrie and Singan, Vasanth and Lindquist, Erika and Ansong, Charles and Purvine, Samuel O. and M. Brewer, Heather and Weyman, Philip D. and Dupont, Christopher L. and Rasmussen, Ulla},
abstractNote = {Dinitrogen (N2)-fixation by cyanobacteria in symbiosis with feathermosses is the primary pathway of biological nitrogen (N) input into boreal forests. Despite its significance, little is known about the cyanobacterial gene repertoire and regulatory rewiring needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions and regulatory changes allowing cyanobacteria to form and maintain this symbiosis, we compared genomically closely related symbiotic-competent and -incompetent Nostoc strains using a proteogenomics approach and an experimental set up allowing for controlled chemical and physical contact between partners. Thirty-two gene families were found only in the genomes of symbiotic strains, including some never before associated with cyanobacterial symbiosis. We identified conserved orthologs that were differentially expressed in symbiotic strains, including protein families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, and glycosyl-modifying and oxidative stress-mediating exoenzymes. The physical moss–cyanobacteria epiphytic symbiosis is distinct from other cyanobacteria–plant symbioses, with Nostoc retaining motility, and lacking modulation of N2-fixation, photosynthesis, GS-GOGAT cycle and heterocyst formation. The results expand our knowledge base of plant–cyanobacterial symbioses, provide a model of information and material exchange in this ecologically significant symbiosis, and suggest new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintaining the cyanobacteria–feathermoss symbiosis.},
doi = {10.1038/ismej.2017.134},
journal = {The ISME Journal},
number = 12,
volume = 11,
place = {United States},
year = {2017},
month = {8}
}

Journal Article:
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Cited by: 11 works
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Figures / Tables:

Figure 1 Figure 1: Nostocales species tree and distribution of HMM occurrences missing in Nostoc sp. CALU 996 (N. 996). (a) Maximum-likelihood phylogeny of Nostocales based on 15 conserved protein comparisons of the five moss symbiotic competent strains sequenced in our study (in blue), the one non-symbiotic competent (in red) and 31more » other Nostocales sequenced during the cyanoGEBA project (Shih et al, 2013). The genomes of Prochlorococcus marinus MED4 and Synechococcus sp. WH8102 were included as outgroups. Bootstrap values (out of 100) are shown at each node. Red boxes show subclades A and B which include the new symbiotic competent strains. (b) Distribution of the HMM occurrences missing in N. 996. Columns in the heat map represent individual gene families (Pfams or TIGRfams) grouped into eight functional protein categories. Increasing representation of each gene family in a given cyanobacteria strain is shown by increasing protein domains counts and depth colour.« less

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