The hidden pangenome: comparative genomics reveals pervasive diversity in symbiotic and free-living sulfur-oxidizing bacteria

Abstract

Sulfur-oxidizing Thioglobaceae, often referred to as SUP05 and Arctic96BD clades, are widespread and common to hydrothermal vents and oxygen minimum zones. They impact global biogeochemical cycles and exhibit a variety of host-associated and free-living lifestyles. The evolutionary driving forces that led to the versatility, adoption of multiple lifestyles and global success of this family are largely unknown. Here, we perform an in-depth comparative genomic analysis using all available and newly generated Thioglobaceae genomes. Gene content variation was common, throughout taxonomic ranks and lifestyles. We uncovered a pool of variable genes within most Thioglobaceae populations in single environmental samples and we referred to this as the ‘hidden pangenome’. The ‘hidden pangenome’ is often overlooked in comparative genomic studies and our results indicate a much higher intra-specific diversity within environmental bacterial populations than previously thought. Our results show that core-community functions are different from species core genomes suggesting that core functions across populations are divided among the intra-specific members within a population. Defense mechanisms against foreign DNA and phages were enriched in symbiotic lineages, indicating an increased exchange of genetic material in symbioses. Our study suggests that genomic plasticity and frequent exchange of genetic material drives the global success of this family by increasing its evolvability in a heterogeneous environment.

Pangenome evolution in environmentally transmitted symbionts of deep-sea mussels is governed by vertical inheritance

“…Whereas the SOX pangenome has less genes than that of MOX, the former has a higher fraction of accessory genes. The large SOX accessory genome is consistent with the recent finding that gene content variation among coexisting thiotrophic bacteria is common (Ansorge et al 2020). We find that functions associated with genome integrity are consistently present in the accessory genomes of both species.…”

Pangenome Evolution in Environmentally Transmitted Symbionts of Deep-Sea Mussels Is Governed by Vertical Inheritance

“…Whereas the SOX pangenome has less genes than that of MOX, the former has a higher fraction of accessory genes. The large SOX accessory genome is consistent with the recent finding that gene content variation among coexisting thiotrophic bacteria is common ( Ansorge et al 2020 ). We found that functions associated with genome plasticity are consistently present in the accessory genomes of both species.…”

“…6 ), whereas HGT with other community members is an exciting direction for future research. SOX belongs to the Thioglobaceae family, which contains many endosymbiotic bacteria that are related to the free-living SUP05 ( Ansorge et al 2020 ). MOX belongs to the Methyloprofundus clade, also containing free-living members ( Hirayama et al 2022 ), which opens the possibility of HGT between closely related species during the free-living phase.…”

Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

“…These proteins are prokaryotic defense mechanisms against bacterial viruses and foreign DNA known to be enriched in the microbiomes of marine sponges [65,73] and octocorals [15]. A recent study of the Thioglobaceae pangenome showed that CRISPR/Cas systems are relatively enriched in mussel, sponge, and scleractinian coral symbionts compared to free-living Thioglobaceae lineages [74]. The Ca.…”