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Mechanisms driving genome reduction of a novel Roseobacter lineage

Summary

Members of the marine Roseobacter group are key players in the global carbon and sulfur cycles. While over 300 species have been described, only 2% possess reduced genomes (mostly 3–3.5 Mbp) compared to an average roseobacter (>4 Mbp). These taxonomic minorities are phylogenetically diverse but form a Pelagic Roseobacter Cluster (PRC) at the genome content level. Here, we cultivated eight isolates constituting a novel Roseobacter lineage which we named ‘CHUG’. Metagenomic and metatranscriptomic read recruitment analyses showed that CHUG members are globally distributed and active in marine pelagic environments. CHUG members possess some of the smallest genomes (~2.6 Mb) among all known roseobacters, but they do not exhibit canonical features of typical bacterioplankton lineages theorized to have undergone genome streamlining processes, like higher coding density, fewer paralogues and rarer pseudogenes. While CHUG members form a genome content cluster with traditional PRC members, they show important differences. Unlike other PRC members, neither the relative abundances of CHUG members nor their relative gene expression levels are correlated with chlorophyll a concentration across the global samples. CHUG members cannot utilize most phytoplankton-derived metabolites or synthesize vitamin B12, a key metabolite mediating the roseobacter-phytoplankton interactions. This combination of features is evidence for the hypothesis that CHUG members may have evolved a free-living lifestyle decoupled from phytoplankton. This ecological transition was accompanied by the loss of signature genes involved in roseobacter-phytoplankton symbiosis, suggesting that relaxation of purifying selection owing to lifestyle shift is likely an important driver of genome reduction in CHUG.

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Fig. 1: Phylogenomic tree and gene content dendrogram of roseobacters.
Fig. 2: Genomic feature comparisons between CHUG, their sister group, the outgroup, seven other PRC members, and other reference roseobacters.
Fig. 3: The global distribution of CHUG and its ecological correlation with environmental factors.
Fig. 4: The phyletic pattern of select genes.
Fig. 5: Growth assay of CHUG strain HKCCA1288 and the model roseobacter Ruegeria pomeroyi DSS-3.

Data availability

Genomic sequences of the eight CHUG genomes are available at the NCBI GenBank database under the accession number PRJNA574877.

Code availability

The custom scripts used in this study are available in the online repository (https://github.com/luolab-cuhk/CHUG-genome-reduction-project).

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Acknowledgements

This research was funded by the National Science Foundation of China (41776129), the Hong Kong Research Grants Council General Research Fund (14163917), the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16), and the Direct Grant of CUHK (4053257 & 3132809). The research was also supported by a Louisiana Board of Regents grant (LEQSF(2014-17)-RD-A-06) and a Simons Early Career Investigator in Marine Microbial Ecology and Evolution Award to JCT.

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Feng, X., Chu, X., Qian, Y. et al. Mechanisms driving genome reduction of a novel Roseobacter lineage. ISME J 15, 3576–3586 (2021). https://doi.org/10.1038/s41396-021-01036-3

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