Mechanisms driving genome reduction of a novel Roseobacter lineage

Abstract

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.

The Influence of Genes on the “Killer Plasmid” of Dinoroseobacter shibae on Its Symbiosis With the Dinoflagellate Prorocentrum minimum

“…D. shibae and several of the more ancient Roseobacters are auxotrophic for biotin, while Phaeobacter and related genera at the other end of the phylogenetic tree can synthesize it (Luo and Moran, 2014). Biotin synthesis genes were also not found in the recently cultivated lineage CUAB that has a streamlined genome (Feng et al, 2021). Accordingly, with respect to biotin, two types of symbioses are possible between algae and Roseobacters in nature, namely between auxotrophic algae (e.g., dinoflagellates) and a certain group of biotin producing Roseobacters, while algae that can synthesize biotin (chlorophyta, haptophytes, diatoms) can form symbioses with the other group of Roseobacters that cannot produce biotin.…”

Bacterial cooperation through horizontal gene transfer

“…Strains that stop performing these costly functions and eventually lose the corresponding genes have a local advantage [15]. While gene loss due to drift is known in bacteria, especially in host-restricted taxa [26,27], genome reduction also occurs in bacteria with very large effective population sizes, such as the marine-dwelling Synechococcus and Roseobacter [28,29]. Selective pressure to lose genes could be due to general genome streamlining caused by deletion bias observed in bacterial genomes [30], a possible way to purge them of selfish genetic elements [31].…”

Coastal Transient Niches Shape the Microdiversity Pattern of a Bacterioplankton Population with Reduced Genomes

“…Here, we isolated 33 strains affiliated with the recently discovered CHUG cluster, a genome-reduced lineage (~2.6 Mbp) ( 21 ) of the globally abundant marine Roseobacter group, which typically contains copiotrophic members with large and variable genomes (>4 Mbp on average) that are commonly associated with phytoplankton groups in the pelagic ocean ( 22 , 23 ). While CHUG genomes are larger than those of the most abundant marine bacterioplankton lineages, such as the alphaproteobacterial SAR11 clade (1.3 to 1.4 Mbp) and the cyanobacterial Prochlorococcus (1.6 to 1.8 Mbp), they are, nevertheless, among the smallest of the Roseobacter genomes.…”

“…While CHUG genomes are larger than those of the most abundant marine bacterioplankton lineages, such as the alphaproteobacterial SAR11 clade (1.3 to 1.4 Mbp) and the cyanobacterial Prochlorococcus (1.6 to 1.8 Mbp), they are, nevertheless, among the smallest of the Roseobacter genomes. The CHUG members differ by up to 1.8% in their 16S rRNA gene sequences, and they together differ from their closest sister group (3.9 Mbp on average) by 3.5% in the same gene ( 21 ). An important consequence of genome reduction is that CHUG members have lost the ability of de novo synthesis of vitamin B 12 ( 21 ).…”

“…The CHUG members differ by up to 1.8% in their 16S rRNA gene sequences, and they together differ from their closest sister group (3.9 Mbp on average) by 3.5% in the same gene ( 21 ). An important consequence of genome reduction is that CHUG members have lost the ability of de novo synthesis of vitamin B 12 ( 21 ). This is unusual because the potential for vitamin B 12 synthesis is widespread among Roseobacter members ( 21 , 22 ) and sets the ground for mutualistic interactions between Roseobacter members and phytoplankton groups that are commonly auxotrophic for vitamin B 12 ( 24 – 26 ), suggesting that phytoplankton may not be an important pelagic niche for CHUG ( 21 ).…”