Metagenomes of Red Sea Subpopulations Challenge the Use of Marker Genes and Morphology to Assess Trichodesmium Diversity

Coco Koedooder, Etai Landou, Futing Zhang, Siyuan Wang, Subhajit Basu, Ilana Berman-Frank, Yeala Shaked, Maxim Rubin-Blum

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5 Scopus citations

Abstract

Trichodesmium are filamentous cyanobacteria of key interest due to their ability to fix carbon and nitrogen within an oligotrophic marine environment. Their blooms consist of a dynamic assemblage of subpopulations and colony morphologies that are hypothesized to occupy unique niches. Here, we assessed the poorly studied diversity of Trichodesmium in the Red Sea, based on metagenome-assembled genomes (MAGs) and hetR gene-based phylotyping. We assembled four non-redundant MAGs from morphologically distinct Trichodesmium colonies (tufts, dense and thin puffs). Trichodesmium thiebautii (puffs) and Trichodesmium erythraeum (tufts) were the dominant species within these morphotypes. While subspecies diversity is present for both T. thiebautii and T. erythraeum, a single T. thiebautii genotype comprised both thin and dense puff morphotypes, and we hypothesize that this phenotypic variation is likely attributed to gene regulation. Additionally, we found the rare non-diazotrophic clade IV and V genotypes, related to Trichodesmium nobis and Trichodesmium miru, respectively that likely occurred as single filaments. The hetR gene phylogeny further indicated that the genotype in clade IV could represent the species Trichodesmium contortum. Importantly, we show the presence of hetR paralogs in Trichodesmium, where two copies of the hetR gene were present within T. thiebautii genomes. This may lead to the overestimation of Trichodesmium diversity as one of the copies misidentified T. thiebautii as Trichodesmium aureum. Taken together, our results highlight the importance of re-assessing Trichodesmium taxonomy while showing the ability of genomics to capture the complex diversity and distribution of Trichodesmium populations.

Original languageEnglish
Article number879970
JournalFrontiers in Microbiology
Volume13
DOIs
StatePublished - 30 May 2022

Bibliographical note

Publisher Copyright:
Copyright © 2022 Koedooder, Landou, Zhang, Wang, Basu, Berman-Frank, Shaked and Rubin-Blum.

Funding

This work was funded by the Israel Science Foundation (260/21) and the Israel-United States Bi-National Science Foundation (2020041) to YS. This work was also financially supported in part by the Schulich Marine Studies Initiative to IB-F. MR-B acknowledges the support of the Israel Science Foundation (913/19), the United States-Israel Binational Science Foundation (2019055), and the Israel Ministry of Science and Technology (1126). FZ thanks the PBC Fellowship Program for Outstanding Chinese and Indian Post-Doctoral Fellows.

FundersFunder number
Israel-United States Bi-National Science Foundation913/19, 2020041
United States-Israel Binational Science Foundation2019055
Israel Science Foundation260/21
Ministry of science and technology, Israel1126

    Keywords

    • Red Sea
    • Trichodesmium
    • biodiversity
    • cyanobacteria
    • hetR
    • metagenome
    • morphotype
    • taxonomy

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