Dataset Information

Linking pangenomes and metagenomes: the Prochlorococcus metapangenome.

ABSTRACT: Pangenomes offer detailed characterizations of core and accessory genes found in a set of closely related microbial genomes, generally by clustering genes based on sequence homology. In comparison, metagenomes facilitate highly resolved investigations of the relative distribution of microbial genomes and individual genes across environments through read recruitment analyses. Combining these complementary approaches can yield unique insights into the functional basis of microbial niche partitioning and fitness, however, advanced software solutions are lacking. Here we present an integrated analysis and visualization strategy that provides an interactive and reproducible framework to generate pangenomes and to study them in conjunction with metagenomes. To investigate its utility, we applied this strategy to a Prochlorococcus pangenome in the context of a large-scale marine metagenomic survey. The resulting Prochlorococcus metapangenome revealed remarkable differential abundance patterns between very closely related isolates that belonged to the same phylogenetic cluster and that differed by only a small number of gene clusters in the pangenome. While the relationships between these genomes based on gene clusters correlated with their environmental distribution patterns, phylogenetic analyses using marker genes or concatenated single-copy core genes did not recapitulate these patterns. The metapangenome also revealed a small set of core genes that mostly occurred in hypervariable genomic islands of the Prochlorococcus populations, which systematically lacked read recruitment from surface ocean metagenomes. Notably, these core gene clusters were all linked to sugar metabolism, suggesting potential benefits to Prochlorococcus from a high sequence diversity of sugar metabolism genes. The rapidly growing number of microbial genomes and increasing availability of environmental metagenomes provide new opportunities to investigate the functioning and the ecology of microbial populations, and metapangenomes can provide unique insights for any taxon and biome for which genomic and sufficiently deep metagenomic data are available.

SUBMITTER: Delmont TO

PROVIDER: S-EPMC5804319 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Linking pangenomes and metagenomes: the <i>Prochlorococcus</i> metapangenome.

Delmont Tom O TO Eren A Murat AM

PeerJ 20180125

Pangenomes offer detailed characterizations of core and accessory genes found in a set of closely related microbial genomes, generally by clustering genes based on sequence homology. In comparison, metagenomes facilitate highly resolved investigations of the relative distribution of microbial genomes and individual genes across environments through read recruitment analyses. Combining these complementary approaches can yield unique insights into the functional basis of microbial niche partitioni ...[more]

PMID: 29423345

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Project description:Evidence suggests many marine bacteria are cosmopolitan, with widespread but sparse strains poised to seed abundant populations under conducive growth conditions. However, studies supporting this "microbial seed bank" hypothesis have analyzed taxonomic marker genes rather than whole genomes/metagenomes, leaving open the possibility that disparate ocean regions harbor endemic gene content. The Red Sea is isolated geographically from the rest of the ocean and has a combination of high irradiance, high temperature, and high salinity that is unique among the oceans; we therefore asked whether it harbors endemic gene content. We sequenced and assembled single-cell genomes of 21 SAR11 (subclades Ia, Ib, Id, and II) and 5 Prochlorococcus (ecotype HLII) samples from the Red Sea and combined them with globally sourced reference genomes to cluster genes into ortholog groups (OGs). Ordination of OG composition could distinguish clades, including phylogenetically cryptic Prochlorococcus ecotypes LLII and LLIII. Compared with reference genomes, 1% of Prochlorococcus and 17% of SAR11 OGs were unique to the Red Sea genomes (RS-OGs). Most (83%) RS-OGs had no annotated function, but 65% of RS-OGs were expressed in diel Red Sea metatranscriptomes, suggesting they are functional. Searching Tara Oceans metagenomes, RS-OGs were as likely to be found as non-RS-OGs; nevertheless, Red Sea and other warm samples could be distinguished from cooler samples using the relative abundances of OGs. The results suggest that the prevalence of OGs in these surface ocean bacteria is largely cosmopolitan, with differences in population metagenomes manifested by differences in relative abundance rather than complete presence/absence of OGs.IMPORTANCE Studies have shown that as we sequence seawater from a selected environment deeper and deeper, we approach finding every bacterial taxon known for the ocean as a whole. However, such studies have focused on taxonomic marker genes rather than on whole genomes, raising the possibility that the lack of endemism results from the method of investigation. We took a geographically isolated water body, the Red Sea, and sequenced single cells from it. We compared those single-cell genomes to available genomes from around the ocean and to ocean-spanning metagenomes. We showed that gene ortholog groups found in Red Sea genomes but not in other genomes are nevertheless common across global ocean metagenomes. These results suggest that Baas Becking's hypothesis "everything is everywhere, but the environment selects" also applies to gene ortholog groups. This widely dispersed functional diversity may give oceanic microbial communities the functional capacity to respond rapidly to changing conditions.

Project description:Prochlorococcus cyanobacteria grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes, including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, the extracellular viability and intracellular infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear whether light-dependent viral life history traits scale up to influence population-level dynamics. Here, we examined the impact of diel forcing on both cellular- and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model, including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence consistent with lysis saturation at relatively high virus-to-cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular-to-population scales.IMPORTANCE The cyanobacterium Prochlorococcus is an essential member of global ocean ecosystems. Light rhythms drive Prochlorococcus photosynthesis, ecology, and interactions with potentially lethal viruses. At present, the impact of light on Prochlorococcus-virus interactions is not well understood. Here, we analyzed Prochlorococcus and virus population dynamics with a light-driven population model and compared our results with experimental data. Our approach revealed that light profoundly drives both cellular- and population-level dynamics for some host-virus systems. However, we also found that additional mechanisms, including lysis saturation, are required to explain observed host-virus dynamics at the population scale. This study provides the basis for future work to understand the intertwined fates of Prochlorococcus and associated viruses in the surface ocean.

Dataset Information

Linking pangenomes and metagenomes: the Prochlorococcus metapangenome.

Publications

Linking pangenomes and metagenomes: the <i>Prochlorococcus</i> metapangenome.

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