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Mechanisms Driving Genome Reduction of a Novel Roseobacter Lineage Showing Vitamin B12 Auxotrophy

Xiaoyuan Feng, Xiao Chu, Yang Qian, Michael W. Henson, V. Celeste Lanclos, Fang Qin, Yanlin Zhao, View ORCID ProfileJ. Cameron Thrash, Haiwei Luo
doi: https://doi.org/10.1101/2021.01.15.426902
Xiaoyuan Feng
1Simon F. S. Li Marine Science Laboratory, School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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Xiao Chu
1Simon F. S. Li Marine Science Laboratory, School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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Yang Qian
1Simon F. S. Li Marine Science Laboratory, School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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Michael W. Henson
2Department of Biological Sciences, University of Southern California, Los Angeles, CA USA
aDepartment of Geophysical Sciences, University of Chicago, Chicago, Illinois, USA
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V. Celeste Lanclos
2Department of Biological Sciences, University of Southern California, Los Angeles, CA USA
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Fang Qin
3Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
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Yanlin Zhao
3Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
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J. Cameron Thrash
2Department of Biological Sciences, University of Southern California, Los Angeles, CA USA
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  • ORCID record for J. Cameron Thrash
Haiwei Luo
1Simon F. S. Li Marine Science Laboratory, School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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  • For correspondence: hluo2006@gmail.com
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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 were globally distributed and active in marine environments. CHUG members possess some of the smallest genomes (~2.52 Mb) among all known roseobacters, but they do not exhibit canonical features of genome streamlining like higher coding density or fewer paralogues and pseudogenes compared to their sister lineages. While CHUG members are clustered with traditional PRC members at the genome content level, they show important differences. Unlike other PRC members, neither the relative abundances of CHUG members nor their gene expression levels are correlated with chlorophyll a concentration across the global samples. Moreover, CHUG members cannot synthesize vitamin B12, a key metabolite made by most roseobacters but not by many phytoplankton species and thus thought to mediate 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 is likely an important driver of genome reduction in CHUG.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 16, 2021.
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Mechanisms Driving Genome Reduction of a Novel Roseobacter Lineage Showing Vitamin B12 Auxotrophy
Xiaoyuan Feng, Xiao Chu, Yang Qian, Michael W. Henson, V. Celeste Lanclos, Fang Qin, Yanlin Zhao, J. Cameron Thrash, Haiwei Luo
bioRxiv 2021.01.15.426902; doi: https://doi.org/10.1101/2021.01.15.426902
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Mechanisms Driving Genome Reduction of a Novel Roseobacter Lineage Showing Vitamin B12 Auxotrophy
Xiaoyuan Feng, Xiao Chu, Yang Qian, Michael W. Henson, V. Celeste Lanclos, Fang Qin, Yanlin Zhao, J. Cameron Thrash, Haiwei Luo
bioRxiv 2021.01.15.426902; doi: https://doi.org/10.1101/2021.01.15.426902

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