Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont

Warshan, Denis; Liaimer, Anton; Pederson, Eric; Kim, Sea-Yong; Shapiro, Nicole; Woyke, Tanja; Altermark, Bjørn; Pawlowski, Katharina; Weyman, Philip D.; Dupont, Christopher L.; Rasmussen, Ulla

doi:10.1093/molbev/msy029

Title: Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont

Journal Article · 15 March 2018 · Molecular Biology and Evolution

DOI: https://doi.org/10.1093/molbev/msy029 · OSTI ID:1434367

^[1]; Liaimer, Anton ^[2]; Pederson, Eric ^[1]; Kim, Sea-Yong ^[1]; Shapiro, Nicole ^[3]; Woyke, Tanja ^[3]; Altermark, Bjørn ^[4]; Pawlowski, Katharina ^[1]; Weyman, Philip D. ^[5]; Dupont, Christopher L. ^[6];

^[1]

Stockholm Univ. (Sweden). Dept. of Ecology, Environment and Plant Sciences
UiT–The Arctic Univ. of Norway, Tromso (Norway). Dept. of Arctic and Marine Biology
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
UiT–The Arctic Univ. of Norway, Tromso (Norway). Dept. of Chemistry
J. Craig Venter Inst., La Jolla, CA (United States). Dept. of Synthetic Biology and Bioenergy
J. Craig Venter Inst., La Jolla, CA (United States). Dept. of Microbial and Environmental Genomics

Cyanobacteria belonging to the genus Nostoc comprise free-living strains and also facultative plant symbionts. Symbiotic strains can enter into symbiosis with taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here, we compared the genomes derived from 11 symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, and inference of transfer events implied that this trait was likely acquired several times in the evolution of the Nostocales. Symbiotic Nostoc strains showed enriched functions in transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, branched-chain amino acids, and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains, with a gain/enrichment of genes encoding proteins to generate L-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell walls. These compounds could function as C-sources for members of the intracellular clade. Molecular clock analysis indicated that the intracellular clade emerged ca. 600 Ma, suggesting that intracellular Nostoc symbioses predate the origin of land plants and the emergence of their extant hosts.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1434367

Alternate ID(s):: OSTI ID: 1543986

Journal Information:: Molecular Biology and Evolution, Vol. 35, Issue 5; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 28 works

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The role of microbial motility and chemotaxis in symbiosis Raina, Jean-Baptiste; Fernandez, Vicente; Lambert, Bennett Nature Reviews Microbiology, Vol. 17, Issue 5 https://doi.org/10.1038/s41579-019-0182-9	journal	March 2019
Cycad Coralloid Roots Contain Bacterial Communities Including Cyanobacteria and Caulobacter spp. That Encode Niche-Specific Biosynthetic Gene Clusters Gutiérrez-García, Karina; Bustos-Díaz, Edder D.; Corona-Gómez, José Antonio Genome Biology and Evolution, Vol. 11, Issue 1 https://doi.org/10.1093/gbe/evy266	journal	December 2018
Complete Genomes of Symbiotic Cyanobacteria Clarify the Evolution of Vanadium-Nitrogenase Nelson, Jessica M.; Hauser, Duncan A.; Gudiño, José A. Genome Biology and Evolution, Vol. 11, Issue 7 https://doi.org/10.1093/gbe/evz137	journal	June 2019
Distinctive characters of Nostoc genomes in cyanolichens Gagunashvili, Andrey N.; Andrésson, Ólafur S. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4743-5	journal	June 2018
Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops Pankievicz, Vânia C. S.; Irving, Thomas B.; Maia, Lucas G. S. BMC Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12915-019-0710-0	journal	December 2019
Genome Sequencing of Pleurozium schreberi : The Assembled and Annotated Draft Genome of a Pleurocarpous Feather Moss Pederson, Eric R. A.; Warshan, Denis; Rasmussen, Ulla G3: Genes\|Genomes\|Genetics, Vol. 9, Issue 9 https://doi.org/10.1534/g3.119.400279	journal	July 2019

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59 BASIC BIOLOGICAL SCIENCES
Biochemistry & Molecular Biology
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cyanobacteria
symbiosis
evolution
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