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Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems.

ABSTRACT: Bacteriophage genomes rapidly evolve via mutation and horizontal gene transfer to counter evolving bacterial host defenses; such arms race dynamics should lead to divergence between phages from similar, geographically isolated ecosystems. However, near-identical phage genomes can reoccur over large geographical distances and several years apart, conversely suggesting many are stably maintained. Here, we show that phages with near-identical core genomes in distant, discrete aquatic ecosystems maintain diversity by possession of numerous flexible gene modules, where homologous genes present in the pan-genome interchange to create new phage variants. By repeatedly reconstructing the core and flexible regions of phage genomes from different metagenomes, we show a pool of homologous gene variants co-exist for each module in each location, however, the dominant variant shuffles independently in each module. These results suggest that in a natural community, recombination is the largest contributor to phage diversity, allowing a variety of host recognition receptors and genes to counter bacterial defenses to co-exist for each phage.

SUBMITTER: Bellas CM

PROVIDER: S-EPMC7468147 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems.

Bellas Christopher M CM Schroeder Declan C DC Edwards Arwyn A Barker Gary G Anesio Alexandre M AM

Nature communications 20200902 1

Bacteriophage genomes rapidly evolve via mutation and horizontal gene transfer to counter evolving bacterial host defenses; such arms race dynamics should lead to divergence between phages from similar, geographically isolated ecosystems. However, near-identical phage genomes can reoccur over large geographical distances and several years apart, conversely suggesting many are stably maintained. Here, we show that phages with near-identical core genomes in distant, discrete aquatic ecosystems mai ...[more]

PMID: 32879312

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Project description:Cryoconite holes are miniature freshwater aquatic ecosystems that harbor a relatively diverse microbial community. This microbial community can withstand the extreme conditions of the supraglacial environment, including fluctuating temperatures, extreme and varying geochemical conditions and limited nutrients. We analyzed the physiological capabilities of microbial isolates from cryoconite holes from Antarctica, Greenland, and Svalbard in selected environmental conditions: extreme pH, salinity, freeze-thaw and limited carbon sources, to identify their physiological limits. The results suggest that heterotrophic microorganisms in cryoconite holes are well adapted to fast-changing environmental conditions, by surviving multiple freeze-thaw cycles, a wide range of salinity and pH conditions and scavenging a variety of organic substrates. Under oxic and anoxic conditions, the communities grew well in temperatures up to 30°C, although in anoxic conditions the community was more successful at colder temperatures (0.2°C). The most abundant cultivable microorganisms were facultative anaerobic bacteria and yeasts. They grew in salinities up to 10% and in pH ranging from 4 to 10.5 (Antarctica), 2.5 to 10 (Svalbard), and 3 to 10 (Greenland). Their growth was sustained on at least 58 single carbon sources and there was no decrease in viability for some isolates after up to 100 consecutive freeze-thaw cycles. The elevated viability of the anaerobic community in the lowest temperatures indicates they might be key players in winter conditions or in early melt seasons, when the oxygen is potentially depleted due to limited flow of meltwater. Consequently, facultative anaerobic heterotrophs are likely important players in the reactivation of the community after the polar night. This detailed physiological investigation shows that despite inhabiting a freshwater environment, cryoconite microorganisms are able to withstand conditions not typically encountered in freshwater environments (namely high salinities or extreme pH), making them physiologically more similar to arid soil communities. The results also point to a possible resilience of the most abundant microorganisms of cryoconite holes in the face of rapid change regardless of the location.

Project description:Antarctic cryoconite holes (CHs) are mostly perennially ice-lidded and sediment-filled depressions that constitute important features on glaciers and ice sheets. Once being hydrologically connected, these microbially dominated mini-ecosystems provide nutrients and biota for downstream environments. For example, the East Antarctic Anuchin Glacier gradually melts into the adjacent perennially ice-covered Lake Untersee, and CH biota from this glacier contribute up to one third of the community composition in benthic microbial mats within the lake. However, biogeochemical features of these CHs and associated spatial patterns across the glacier are still unknown. Here we hypothesized about the CH minerogenic composition between the different sources such as the medial moraine and other zones. Further, we intended to investigate if the depth of the CH mirrors the CH community composition, organic matter (OM) content and would support productivity. In this study we show that both microbial communities and biogeochemical parameters in CHs were significantly different between the zones medial moraine and the glacier terminus. Variations in microbial community composition are the result of factors such as depth, diameter, organic matter, total carbon, particle size, and mineral diversity. More than 90% of all ribosomal sequence variants (RSV) reads were classified as Proteobacteria, Cyanobacteria, Bacteroidetes, Actinobacteria, and Acidobacteria. Archaea were detected in 85% of all samples and exclusively belonged to the classes Halobacteria, Methanomicrobia, and Thermoplasmata. The most abundant genus was Halorubrum (Halobacteria) and was identified in nine RSVs. The core microbiome for bacteria comprised 30 RSVs that were affiliated with Cyanobacteria, Bacteroidetes, Actinobacteria, and Proteobacteria. The archaeal fraction of the core microbiome consisted of three RSVs belonging to unknown genera of Methanomicrobiales and Thermoplasmatales and the genus Rice_Cluster_I (Methanocellales). Further, mean bacterial carbon production in cryoconite was exceptionally low and similar rates have not been reported elsewhere. However, bacterial carbon production insignificantly trended toward higher rates in shallow CHs and did not seem to be supported by accumulation of OM and nutrients, respectively, in deeper holes. OM fractions were significantly different between shallower CHs along the medial moraine and deeper CHs at the glacier terminus. Overall, our findings suggest that wind-blown material originating south and southeast of the Anuchin Glacier and deposits from a nunatak are assumed to be local inoculation sources. High sequence similarities between samples from the Untersee Oasis and other Antarctic sites further indicate long-range atmospheric transport mechanisms that complement local inoculation sources.

Dataset Information

Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems.

Publications

Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems.

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