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Metagenomic analysis of viral and microbial communities from global high-latitude pristine environments as a model to understand the influence of viruses on the ecosystem

Final Report Summary - COOLVIROMES (Metagenomic analysis of viral and microbial communities from global high-latitude pristine environments as a model to understand the influence of viruses on the ecosystem)

Viruses constitute the most abundant biological entities and a large reservoir of genetic diversity on Earth. They have been shown to control microbial communities and influence host evolution. Moreover, viruses are able to exert a profound effect on food-web interactions and hence affect global geochemical cycles. Experimental and environmental data pointing to an enormous and largely underestimated importance of viruses in ecosystem’s functioning continue to accumulate. However, their influence in ecosystems is still poorly understood. Similarly to other microorganisms, the study of viruses has been largely limited by the constraints of isolation and laboratory culture of viruses and their hosts found in nature. Additionally, the study of viruses has been historically focused on understanding how viruses produce diseases in humans, domestic animals and plants. As a consequence, we know essentially nothing about most of the viruses in nature (Suttle, Nat. Rev. Microbiol. 5: 801. 2007).

Metagenomics is a rapidly expanding science which attempts to understand biology at the aggregate level, transcending the individual organism to focus on the genes in the community (Dinsdale et al., Nature 452: 629. 2008). Coupled to the use of next generation sequencing (NGS) the Metagenomics-NGS approach has been able to surpass previous limitations to the study of environmental viruses. However, despite the recent increased interest in environmental viruses, our knowledge remains sparse. We are still only scratching the surface of discovery of global viral diversity, have little understanding of the functionality of the majority of genes in the global viral gene pool and the roles they play in the interaction with their hosts, and are still grappling with understanding viral impact on ecological and evolutionary processes (Rohwer et al., Environ. Microbiol. 11: 2771. 2009).

During 2006, members of the host group participated in a scientific expedition to Antarctica, with the goal of studying the genetic diversity of native viral communities of freshwater Antarctic environments. They employed a Metagenomics-NGS approach and found an unexpected viral diversity for such an extreme and high latitude ecosystem with thousands of viral species distributed along the highest number of viral families detected in aquatic ecosystems so far. This study represented the first genetic identification of any virus in Antarctic habitats and the first viral metagenome published by a European team.

Pristine, high-latitude freshwater ecosystems represent some of the last unaltered habitats on the planet (Convey et al., Science 317: 1877. 2007). These ecosystems commonly present limited nutrient input and are dominated by microorganisms, commonly presenting very small meso- and macroorganism communities, which translates into relatively simple natural ecosystems with short food-webs. This research project was based on the recognition that due to their relative simplicity, these habitats constitute a unique ecological model to understand the influence of viruses on natural microbial communities and the overall ecosystem. With this background, this research project used Metagenomics and NGS techniques, as well as state-of-the-art computational approaches, to analyze the genetic diversity of viral communities, as well as the structure of viral and microbial communities, in pristine high-latitude freshwater habitats.

The project also presented a strong transfer of knowledge component, aiming to complement and enhance the host’s knowledge and experience in the use of NGS and novel Metagenomics approaches, and specially in related bioinformatics and analytical techniques to study microbial communities, augmenting their ability to produce high-impact science.

We conducted in-depth metagenomic analyses of Arctic freshwater microbial communities, and comparative meta-analyses with other freshwater environments previously described. Arctic viromes were dominated by unknown and single-stranded DNA viruses with no close relatives in the database. These unique viral communities mostly relate to each other and present some minor genetic overlap with other environments studied. Despite common environmental conditions in Polar ecosystems, the Arctic and Antarctic viromes differ at the fine grain genetic level while sharing a similar taxonomic composition. The study uncovered some microbial lineages with a bi-polar distribution, suggesting a global dispersal capacity for microorganisms, and seemingly indicated that microbes may not follow the latitudinal diversity gradient known for macroorganisms.

A subsequent study analyzing viral assemblages in freshwater bodies along a latitudinal transect of the Antarctic Peninsula sustained that both polar regions present viral communities similar at a broad taxonomic level but significantly different at the fine scale. Also, we observed no indication of there being a reduction in either viral richness or diversity estimates with increasing latitude, further adding to the controversy regarding the possible existence of latitudinal diversity gradients in the microbial world. To extend these studies, we participated in the Spanish Antarctic Campaign in January 2015 to sample other lakes in Byers Peninsula (Livingston Island). These samples will be of high relevance to extend these studies to other Antarctic freshwater ecosystems.

Later, we produced an assessment of the three layers of microbial life: bacteria, microeukaryotes, and T4-like myoviruses, in the studied ecosystems. Overall the percentages of taxa shared among sites were remarkable, indicating that many microbial taxa are globally-distributed. We found significant correlations between community structures of the different layers, as well as between bacterial and microeukaryotic community structures and recorded physicochemical parameters, which seemingly indicates that environmental filtering is the main factor driving community structure, with biogeographical patterns appearing only at larger scales

Finally, we also employed diverse in silico simulated viromes to evaluate how extensively viral genomes can be assembled using different sequencing platforms and assemblers, and investigated the suitability of different methods to estimate viral diversity in metagenomes.

Collectively, the results derived from this research project have provided a wider understanding of the diversity and structure of polar lacustrine microbial communities, the complexity of their biotic interactions, and shed light into the global biogeography and connectivity of microbial communities.