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Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium.

ABSTRACT: Symbiotic N₂-fixing microorganisms have a crucial role in the assimilation of nitrogen by eukaryotes in nitrogen-limited environments^1-3. Particularly among land plants, N₂-fixing symbionts occur in a variety of distantly related plant lineages and often involve an intimate association between host and symbiont^2,4. Descriptions of such intimate symbioses are lacking for seagrasses, which evolved around 100 million years ago from terrestrial flowering plants that migrated back to the sea⁵. Here we describe an N₂-fixing symbiont, 'Candidatus Celerinatantimonas neptuna', that lives inside seagrass root tissue, where it provides ammonia and amino acids to its host in exchange for sugars. As such, this symbiosis is reminiscent of terrestrial N₂-fixing plant symbioses. The symbiosis between Ca. C. neptuna and its host Posidonia oceanica enables highly productive seagrass meadows to thrive in the nitrogen-limited Mediterranean Sea. Relatives of Ca. C. neptuna occur worldwide in coastal ecosystems, in which they may form similar symbioses with other seagrasses and saltmarsh plants. Just like N₂-fixing microorganisms might have aided the colonization of nitrogen-poor soils by early land plants⁶, the ancestors of Ca. C. neptuna and its relatives probably enabled flowering plants to invade nitrogen-poor marine habitats, where they formed extremely efficient blue carbon ecosystems⁷.

SUBMITTER: Mohr W

PROVIDER: S-EPMC8636270 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium.

Mohr Wiebke W Lehnen Nadine N Ahmerkamp Soeren S Marchant Hannah K HK Graf Jon S JS Tschitschko Bernhard B Yilmaz Pelin P Littmann Sten S Gruber-Vodicka Harald H Leisch Nikolaus N Weber Miriam M Lott Christian C Schubert Carsten J CJ Milucka Jana J Kuypers Marcel M M MMM

Nature 20211103 7887

Symbiotic N2-fixing microorganisms have a crucial role in the assimilation of nitrogen by eukaryotes in nitrogen-limited environments1-3. Particularly among land plants, N2-fixing symbionts occur in a variety of distantly related plant lineages and often involve an intimate association between host and symbiont2,4. Descriptions of such intimate symbioses are lacking for seagrasses, which evolved around 100 million years ago from terrestrial flowering p ...[more]

PMID: 34732889

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Project description:Differences in genome size and gene content are among the most important signatures of microbial adaptation and genome evolution. Here, we investigated the patterns of genome variation among strains of the symbiotic nitrogen-fixing bacterium Sinorhizobium meliloti. Using the sequenced strain Rm1021 as a reference, the genome size and gene content variations were analyzed among ten diverse natural strains, through pulse field gel electrophoresis (PFGE) and whole-genome microarray hybridizations. Our PFGE analysis showed a genome size range of 6.45-7.01Mbp, with the greatest variation arising from the pSymA replicon, followed by that of pSymB. No observable size difference was evident among the chromosomes. Consistent with this pattern of size differences, 41.2% of ORFs on pSymA were variably absent/present, followed by 12.7% on pSymB, and 3.7% on the chromosome. However, the percentages of ORFs that were variably duplicated were more evenly distributed among the three replicons, 11.0%, 16.5% and 15.3% respectively for ORFs on pSymA, pSymB and the chromosome. Among the 10 strains, the percentages of absent ORFs ranged from 1.51% to 6.35% and those of duplicated ORFs ranged from 0.27% to 8.56%. Our analyses showed that host plants, geographic origins, multilocus enzyme electrophoretic types, and replicon sizes had little influence on the distribution patterns of absent or duplicated ORFs. The proportions of ORFs that were either variably absent/present or variably duplicated differed greatly among the functional categories, for each of the three replicons as well as for the whole genome. Interestingly, we observed positive correlations among the three replicons in their numbers of absent ORFs as well as the numbers of duplicated ORFs, consistent with coordinated gene gains/losses in this important bacterium in nature. microarray:Sm6kOligo A total of 12 strains were included for the microarray analyses in this study. The 12 strains included two reference strains and ten other natural strains. Reference strain Rm1021 was the strain with a completely sequenced genome, from which the whole genome microarray was based on (Krol et al. 2004). The second reference strain RmF909 was derived from strain Rm1021 but with a deletion of 575 ORFs located on the megaplasmid pSymB (genomic location 106724-735431, Charles et al. 1991). The two reference strains were used for positive and negative controls in our microarray hybridization experiments and for establishing threshold values for determining whether an ORF is present or absent among natural strains.

Dataset Information

Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium.

Publications

Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium.

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