Fundamental differences in diversity and genomic population structure between Atlantic and Pacific Prochlorococcus

Abstract

The Atlantic and Pacific Oceans represent different biogeochemical regimes in which the abundant marine cyanobacterium Prochlorococcus thrives. We have shown that Prochlorococcus populations in the Atlantic are composed of hundreds of genomically, and likely ecologically, distinct coexisting subpopulations with distinct genomic backbones. Here we ask if differences in the ecology and selection pressures between the Atlantic and Pacific are reflected in the diversity and genomic composition of their indigenous Prochlorococcus populations. We applied large-scale single-cell genomics and compared the cell-by-cell genomic composition of wild populations of co-occurring cells from samples from Station ALOHA off Hawaii, and from Bermuda Atlantic Time Series Station off Bermuda. We reveal fundamental differences in diversity and genomic structure of populations between the sites. The Pacific populations are more diverse than those in the Atlantic, composed of significantly more coexisting subpopulations and lacking dominant subpopulations. Prochlorococcus from the two sites seem to be composed of mostly non-overlapping distinct sets of subpopulations with different genomic backbones-likely reflecting different sets of ocean-specific micro-niches. Furthermore, phylogenetically closely related strains carry ocean-associated nutrient acquisition genes likely reflecting differences in major selection pressures between the oceans. This differential selection, along with geographic separation, clearly has a significant role in shaping these populations.

Unlocking the genomic taxonomy of theProchlorococcuscollective

“…Overall, we demonstrated that the methods used (AAI, core protein sequences and MLSA) correlated and provided significant taxonomic resolution for differentiation of genera and species in PC (Figure 2 and 3). The proposed genera are in complete agreement with previous literature and support previous theories on the evolution of Prochlorococcus [11,13,14,19,45,47,50]. The PC genomic signatures were more similar between closely related species than distantly related species.…”

“…First, the GC% content of the genomes was determined. A phylogenomic framework was established using genomic signatures, 13 i.e., average amino acid identity (AAI), MLSA and core genome-based tree. We then classified the genomes into different genera and species using relevant AAI and phenotypic information obtained directly from the genomes.…”

“…They argued that such a large set of coexisting species with distinct genomic backbones is a characteristic feature of freeliving prokaryotes with very large population sizes living in highly mixed habitats. In another study by these authors focused on the Pacific Ocean, they concluded that the Atlantic and Pacific Oceans are occupied by different PC populations that experienced separate evolutionary paths for a few million years [13].…”

Intra-species diversity ensures the maintenance of functional microbial communities under changing environmental conditions

“…Several studies have described the existence of ecotypes within microbial species in several environments such as host-associated microbiomes [20-22, 28, 29, 75], granular biofilms [76], marshes [22], the ocean [12,34,77,78], oil spills [30,31] or freshwater lakes [79][80][81][82]. Moreover, it has been claimed that a rich biodiversity guarantees the long-lasting maintenance of bacterial populations [33,39,83,84].…”

“…The existence of ecotypes with overlapping ecological functions (but adapted to different niches) has been proposed to confer stability to microbial ecosystems [32], guaranteeing the long-lasting persistence of bacterial populations [33]. Indeed, several species have been shown to consist of many different subpopulations that sustain their distribution across broad environmental gradients [12,30,31,34]. However, it is still not clear whether this intra-species diversity also contributes to the preservation of the higher order inter-species interactions that are fundamental for community functioning and stability.…”