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

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

doi:10.1038/ismej.2017.134

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

Journal Article · Fri Aug 11 00:00:00 EDT 2017 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2017.134· OSTI ID:1409934

Warshan, Denis ^[1]; Espinoza, Josh L. ^[2]; Stuart, Rhona K. ^[3]; Richter, R. Alexander ^[2]; Kim, Sea-Yong ^[1]; Shapiro, Nicole ^[4]; Woyke, Tanja ^[4]; C. Kyrpides, Nikos ^[4]; Barry, Kerrie ^[4]; ^[4]; Lindquist, Erika ^[4]; Ansong, Charles ^[5]; Purvine, Samuel O. ^[6]; ^[6]; Weyman, Philip D. ^[2]; Dupont, Christopher L. ^[2]; Rasmussen, Ulla ^[1]

Stockholm Univ. (Sweden). Department of Ecology, Environment and Plant Sciences
J Craig Venter Institute, La Jolla, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC52-07NA27344; AC02-05CH11231; AC05-76RL01830

OSTI ID:: 1409934

Alternate ID(s):: OSTI ID: 1422344
OSTI ID: 1430726

Report Number(s):: LLNL-JRNL--730832

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 12 Vol. 11; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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