Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation

Abstract

Cyanobacteria are photosynthetic prokaryotes that inhabit diverse aquatic and terrestrial environments. However, the evolutionary mechanisms involved in the cyanobacterial habitat adaptation remain poorly understood. Here, based on phylogenetic and comparative genomic analyses of 650 cyanobacterial genomes, we investigated the genetic basis of cyanobacterial habitat adaptation (marine, freshwater, and terrestrial). We show: (1) the expansion of gene families is a common strategy whereby terrestrial cyanobacteria cope with fluctuating environments, whereas the genomes of many marine strains have undergone contraction to adapt to nutrient-poor conditions. (2) Hundreds of genes are strongly associated with specific habitats. Genes that are differentially abundant in genomes of marine, freshwater, and terrestrial cyanobacteria were found to be involved in light sensing and absorption, chemotaxis, nutrient transporters, responses to osmotic stress, etc., indicating the importance of these genes in the survival and adaptation of organisms in specific habitats. (3) A substantial fraction of genes that facilitate the adaptation of Cyanobacteria to specific habitats are contributed by horizontal gene transfer, and such genetic exchanges are more frequent in terrestrial cyanobacteria. Collectively, our results further our understandings of the adaptations of Cyanobacteria to different environments, highlighting the importance of ecological constraints imposed by the environment in shaping the evolution of Cyanobacteria.

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Fig. 1: Phylogenomics of Cyanobacteria phyla.
Fig. 2: A genome-wide comparison of marine, freshwater, and terrestrial strains.
Fig. 3: Distribution of genes associated with light sensing and absorption across marine, freshwater, and terrestrial genomes.
Fig. 4: A representative set of genes enriched in specific habitats.
Fig. 5: Predicted HGT events across the Cyanobacteria tree of life.
Fig. 6: Horizontal gene transfer events with habitat-specific activity facilitated the enrichment of gene families from specific ecosystem.

Data availability

Cyanobacterial strains reported in this study could be found and ordered in Freshwater Algae Culture Collection at the Institute of Hydrobiology, China (http://algae.ihb.ac.cn/english/Cultrues.aspx). The genomes reported in this study are publicly available from the NCBI Bioproject database under the accession number PRJNA598298. The high-resolution phylogenetic trees of Cyanobacteria based on the BUSCO dataset and multigene dataset were deposited on iTOL (https://itol.embl.de/tree/1836397239155351578467673, https://itol.embl.de/tree/1836397145361531569311402). Additional analytic results are available through figshare (https://figshare.com/s/6b64fa50e1fa720e3587).

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Acknowledgements

This project was supported by the National Natural Science Foundation of China (NSFC) grants 31900002 and 41830318. We thank C. He and J.L. Liang for discussions on the results and comments on the manuscript.

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Correspondence to Bo-Ping Han or Li-Rong Song or Wen-Sheng Shu.

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Chen, M., Teng, W., Zhao, L. et al. Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation. ISME J (2020). https://doi.org/10.1038/s41396-020-00775-z

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