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

Journal Article · · The ISME Journal (Online)
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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.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Organization:
USDOE
DOE Contract Number:
AC05-76RL01830
OSTI ID:
1422344
Report Number(s):
PNNL-SA-127738; 48081; KP1704020
Journal Information:
The ISME Journal (Online), Vol. 11, Issue 12; Related Information: 2821–2833; ISSN 1751-7370
Country of Publication:
United States
Language:
English

References (51)

A Hormogonium Regulating Locus, hrmUA , of the Cyanobacterium Nostoc punctiforme Strain ATCC 29133 and its Response to an Extract of a Symbiotic Plant Partner Anthoceros punctatus March 1997
Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera December 2009
Comparative transcriptomics with a motility-deficient mutant leads to identification of a novel polysaccharide secretion system in Nostoc punctiforme : Gliding motility associated with polysaccharide secretion January 2013
Ecosystem Feedbacks and Nitrogen Fixation in Boreal Forests May 2008
Legume pectate lyase required for root infection by rhizobia December 2011
Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems November 2016
Global Gene Expression Patterns of Nostoc punctiforme in Steady-State Dinitrogen-Grown Heterocyst-Containing Cultures and at Single Time Points during the Differentiation of Akinetes and Hormogonia May 2007
DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra February 2008
Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria March 1979
The Role of Bryophytes in Carbon and Nitrogen Cycling September 2003
Nitric Oxide Mediates Biofilm Formation and Symbiosis in Silicibacter sp. Strain TrichCH4B May 2015
The Nitric Oxide Production in the Moss Physcomitrella patens Is Mediated by Nitrate Reductase March 2015
Quantifying nitrogen-fixation in feather moss carpets of boreal forests October 2002
AutoSOME: a clustering method for identifying gene expression modules without prior knowledge of cluster number March 2010
Multiple Roles of Soluble Sugars in the Establishment of Gunnera - Nostoc Endosymbiosis September 2010
Gimme shelter: how Vibrio fischeri successfully navigates an animal’s multiple environments January 2013
Cyanobacterial reuse of extracellular organic carbon in microbial mats October 2015
Global Transcription Profiles of the Nitrogen Stress Response Resulting in Heterocyst or Hormogonium Development in Nostoc punctiforme October 2011
Biological nitrogen fixation in non-legume plants March 2013
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing December 2012
A scaling normalization method for differential expression analysis of RNA-seq data March 2010
MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC–MS(/MS) features June 2008
The resilience and functional role of moss in boreal and arctic ecosystems: Tansley review August 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies January 2014
Early Communication in the Gunnera - Nostoc Symbiosis: Plant-Induced Cell differention and Protein Systhesis in the Cyanobacterium January 1994
Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria March 2008
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data November 2009
Evidence that a modified type IV pilus-like system powers gliding motility and polysaccharide secretion in filamentous cyanobacteria: Gliding motility and polysaccharide secretion in filamentous cyanobacteria October 2015
Boreal feather mosses secrete chemical signals to gain nitrogen June 2013
Symbiosis between the cyanobacterium Nostoc and the liverwort Blasia requires a CheR-type MCP methyltransferase December 2012
Accelerated Profile HMM Searches October 2011
Across-Habitat Comparison of Diazotroph Activity in the Subarctic November 2014
Microbial pectate lyases: characterization and enzymological properties October 2008
Cryptic carbon and sulfur cycling between surface ocean plankton December 2014
Molecular Analysis of Genes in Nostoc punctiforme Involved in Pilus Biogenesis and Plant Infection April 2007
Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme December 2014
A simple, fast, and accurate method of phylogenomic inference January 2008
DNA Microarray Comparisons of Plant Factor- and Nitrogen Deprivation-Induced Hormogonia Reveal Decision-Making Transcriptional Regulation Patterns in Nostoc punctiforme September 2008
The Bryosphere: An Integral and Influential Component of the Earth’s Biosphere May 2010
Cyanobacteria-bryophyte symbioses February 2008
DNA binding properties of the HrmR protein of Nostoc punctiforme responsible for transcriptional regulation of genes involved in the differentiation of hormogonia: DNA binding protein, HrmR, of Nostoc punctiforme January 2003
Genetic characterization of the hmp locus, a chemotaxis-like gene cluster that regulates hormogonium development and motility in N ostoc punctiforme : Characterization of the March 2014
Regulation of Cellular Differentiation in Filamentous Cyanobacteria in Free-Living and Plant-Associated Symbiotic Growth States March 2002
Environmental Factors and Ecological Processes in Boreal Forests November 1989
MS-GF+ makes progress towards a universal database search tool for proteomics October 2014
Symbiosis between Nitrogen-Fixing Cyanobacteria and Plants April 1998
Functional distinctness in the exoproteomes of marine S ynechococcus : Exoproteomes of marine April 2015
Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage December 2011
VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data January 2015
Imprints of independent allopolyploid formations on patterns of gene expression in two sibling yarrow species (Achillea, Asteraceae) April 2021
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies January 2014

Cited By (9)

Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean July 2019
The future of genomics in polar and alpine cyanobacteria February 2018
Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont March 2018
Differential gene expression associated with fungal trophic shifts along the senescence gradient of the moss Dicranum scoparium April 2019
Distinctive characters of Nostoc genomes in cyanolichens June 2018
Genome Sequencing of Pleurozium schreberi : The Assembled and Annotated Draft Genome of a Pleurocarpous Feather Moss July 2019
A plant perspective on nitrogen cycling in the rhizosphere March 2019
Novel bacterial lineages associated with boreal moss species July 2018
Widespread occurrence and unexpected diversity of red‐shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems March 2019

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