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

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)
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. https://doi.org/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. https://doi.org/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 = {},
doi = {10.1038/ismej.2017.134},
journal = {The ISME Journal},
number = 12,
volume = 11,
place = {United States},
year = {Fri Aug 11 00:00:00 EDT 2017},
month = {Fri Aug 11 00:00:00 EDT 2017}
}

Journal Article:
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Citation Metrics:
Cited by: 35 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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Works referenced in this record:

Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera
journal, December 2009


Ecosystem Feedbacks and Nitrogen Fixation in Boreal Forests
journal, May 2008


Legume pectate lyase required for root infection by rhizobia
journal, December 2011

  • Xie, F.; Murray, J. D.; Kim, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 2
  • DOI: 10.1073/pnas.1113992109

Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems
journal, November 2016

  • Rousk, Kathrin; Degboe, Jefferson; Michelsen, Anders
  • New Phytologist, Vol. 214, Issue 1
  • DOI: 10.1111/nph.14331

DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra
journal, February 2008


Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria
journal, March 1979

  • Stanier, Roger Y.; Deruelles, Josette; Rippka, Rosmarie
  • Microbiology, Vol. 111, Issue 1, p. 1-61
  • DOI: 10.1099/00221287-111-1-1

The Role of Bryophytes in Carbon and Nitrogen Cycling
journal, September 2003

  • Turetsky, Merritt R.
  • The Bryologist, Vol. 106, Issue 3
  • DOI: 10.1639/05

Nitric Oxide Mediates Biofilm Formation and Symbiosis in Silicibacter sp. Strain TrichCH4B
journal, May 2015


The Nitric Oxide Production in the Moss Physcomitrella patens Is Mediated by Nitrate Reductase
journal, March 2015

  • Medina-Andrés, Rigoberto; Solano-Peralta, Alejandro; Saucedo-Vázquez, Juan Pablo
  • PLOS ONE, Vol. 10, Issue 3
  • DOI: 10.1371/journal.pone.0119400

Quantifying nitrogen-fixation in feather moss carpets of boreal forests
journal, October 2002

  • DeLuca, Thomas H.; Zackrisson, Olle; Nilsson, Marie-Charlotte
  • Nature, Vol. 419, Issue 6910
  • DOI: 10.1038/nature01051

AutoSOME: a clustering method for identifying gene expression modules without prior knowledge of cluster number
journal, March 2010


Multiple Roles of Soluble Sugars in the Establishment of Gunnera - Nostoc Endosymbiosis
journal, September 2010

  • Khamar, Hima J.; Breathwaite, Erick K.; Prasse, Christine E.
  • Plant Physiology, Vol. 154, Issue 3
  • DOI: 10.1104/pp.110.162529

Gimme shelter: how Vibrio fischeri successfully navigates an animal’s multiple environments
journal, January 2013


Cyanobacterial reuse of extracellular organic carbon in microbial mats
journal, October 2015

  • Stuart, Rhona K.; Mayali, Xavier; Lee, Jackson Z.
  • The ISME Journal, Vol. 10, Issue 5
  • DOI: 10.1038/ismej.2015.180

Global Transcription Profiles of the Nitrogen Stress Response Resulting in Heterocyst or Hormogonium Development in Nostoc punctiforme
journal, October 2011

  • Christman, H. D.; Campbell, E. L.; Meeks, J. C.
  • Journal of Bacteriology, Vol. 193, Issue 24
  • DOI: 10.1128/JB.05999-11

Biological nitrogen fixation in non-legume plants
journal, March 2013

  • Santi, Carole; Bogusz, Didier; Franche, Claudine
  • Annals of Botany, Vol. 111, Issue 5
  • DOI: 10.1093/aob/mct048

Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing
journal, December 2012

  • Shih, P. M.; Wu, D.; Latifi, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058
  • DOI: 10.1073/pnas.1217107110

A scaling normalization method for differential expression analysis of RNA-seq data
journal, March 2010


MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC–MS(/MS) features
journal, June 2008


The resilience and functional role of moss in boreal and arctic ecosystems: Tansley review
journal, August 2012


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Early Communication in the Gunnera - Nostoc Symbiosis: Plant-Induced Cell differention and Protein Systhesis in the Cyanobacterium
journal, January 1994

  • Rasmussen, Ulla
  • Molecular Plant-Microbe Interactions, Vol. 7, Issue 6
  • DOI: 10.1094/MPMI-7-0696

Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria
journal, March 2008

  • Papaefthimiou, D.; Hrouzek, P.; Mugnai, M. A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 3
  • DOI: 10.1099/ijs.0.65312-0

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


Boreal feather mosses secrete chemical signals to gain nitrogen
journal, June 2013

  • Bay, Guillaume; Nahar, Nurun; Oubre, Matthieu
  • New Phytologist, Vol. 200, Issue 1
  • DOI: 10.1111/nph.12403

Symbiosis between the cyanobacterium Nostoc and the liverwort Blasia requires a CheR-type MCP methyltransferase
journal, December 2012


Accelerated Profile HMM Searches
journal, October 2011


Across-Habitat Comparison of Diazotroph Activity in the Subarctic
journal, November 2014


Microbial pectate lyases: characterization and enzymological properties
journal, October 2008

  • Payasi, Anurag; Sanwal, Rajni; Sanwal, G. G.
  • World Journal of Microbiology and Biotechnology, Vol. 25, Issue 1
  • DOI: 10.1007/s11274-008-9870-8

Cryptic carbon and sulfur cycling between surface ocean plankton
journal, December 2014

  • Durham, Bryndan P.; Sharma, Shalabh; Luo, Haiwei
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1413137112

Molecular Analysis of Genes in Nostoc punctiforme Involved in Pilus Biogenesis and Plant Infection
journal, April 2007

  • Duggan, P. S.; Gottardello, P.; Adams, D. G.
  • Journal of Bacteriology, Vol. 189, Issue 12
  • DOI: 10.1128/JB.01927-06

Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme
journal, December 2014

  • Campbell, Elsie L.; Hagen, Kari D.; Chen, Rui
  • Journal of Bacteriology, Vol. 197, Issue 4
  • DOI: 10.1128/JB.02374-14

A simple, fast, and accurate method of phylogenomic inference
journal, January 2008


The Bryosphere: An Integral and Influential Component of the Earth’s Biosphere
journal, May 2010


Cyanobacteria-bryophyte symbioses
journal, February 2008

  • Adams, D. G.; Duggan, P. S.
  • Journal of Experimental Botany, Vol. 59, Issue 5
  • DOI: 10.1093/jxb/ern005

Regulation of Cellular Differentiation in Filamentous Cyanobacteria in Free-Living and Plant-Associated Symbiotic Growth States
journal, March 2002


Environmental Factors and Ecological Processes in Boreal Forests
journal, November 1989


MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014

  • Kim, Sangtae; Pevzner, Pavel A.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6277

Symbiosis between Nitrogen-Fixing Cyanobacteria and Plants
journal, April 1998


Functional distinctness in the exoproteomes of marine S ynechococcus : Exoproteomes of marine
journal, April 2015

  • Christie-Oleza, Joseph A.; Armengaud, Jean; Guerin, Philippe
  • Environmental Microbiology, Vol. 17, Issue 10
  • DOI: 10.1111/1462-2920.12822

Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage
journal, December 2011

  • Dupont, Chris L.; Rusch, Douglas B.; Yooseph, Shibu
  • The ISME Journal, Vol. 6, Issue 6
  • DOI: 10.1038/ismej.2011.189

VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data
journal, January 2015


Works referencing / citing this record:

Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean
journal, July 2019

  • Durham, Bryndan P.; Boysen, Angela K.; Carlson, Laura T.
  • Nature Microbiology, Vol. 4, Issue 10
  • DOI: 10.1038/s41564-019-0507-5

The future of genomics in polar and alpine cyanobacteria
journal, February 2018

  • Chrismas, Nathan A. M.; Anesio, Alexandre M.; Sánchez-Baracaldo, Patricia
  • FEMS Microbiology Ecology, Vol. 94, Issue 4
  • DOI: 10.1093/femsec/fiy032

Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont
journal, March 2018

  • Warshan, Denis; Liaimer, Anton; Pederson, Eric
  • Molecular Biology and Evolution, Vol. 35, Issue 5
  • DOI: 10.1093/molbev/msy029

Differential gene expression associated with fungal trophic shifts along the senescence gradient of the moss Dicranum scoparium
journal, April 2019

  • Chen, Ko‐Hsuan; Liao, Hui‐Ling; Bellenger, Jean‐Philippe
  • Environmental Microbiology, Vol. 21, Issue 7
  • DOI: 10.1111/1462-2920.14605

Distinctive characters of Nostoc genomes in cyanolichens
journal, June 2018


Genome Sequencing of Pleurozium schreberi : The Assembled and Annotated Draft Genome of a Pleurocarpous Feather Moss
journal, July 2019

  • Pederson, Eric R. A.; Warshan, Denis; Rasmussen, Ulla
  • G3: Genes|Genomes|Genetics, Vol. 9, Issue 9
  • DOI: 10.1534/g3.119.400279

A plant perspective on nitrogen cycling in the rhizosphere
journal, March 2019

  • Moreau, Delphine; Bardgett, Richard D.; Finlay, Roger D.
  • Functional Ecology, Vol. 33, Issue 4
  • DOI: 10.1111/1365-2435.13303

Novel bacterial lineages associated with boreal moss species
journal, July 2018

  • Holland‐Moritz, Hannah; Stuart, Julia; Lewis, Lily R.
  • Environmental Microbiology, Vol. 20, Issue 7
  • DOI: 10.1111/1462-2920.14288

Widespread occurrence and unexpected diversity of red‐shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems
journal, March 2019

  • Zhang, Zhong‐Chun; Li, Zheng‐Ke; Yin, Yan‐Chao
  • Environmental Microbiology, Vol. 21, Issue 4
  • DOI: 10.1111/1462-2920.14582

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