Microbial evolution in extreme environments: microbial migration, genomic highways, and geochemical barriers in hydrothermal ecosystems

摘要

Background Recent advances in microbial ecology are providing unprecedented opportunities to test Baas Becking’s oft-cited “everything is everywhere, environment selects” axiom. A number of recent studies have brought together genomic, ecological, and physico-chemical approaches that are, for the first time, beginning to test and quantify this axiom, providing fundamental shifts in our understanding of microbial ecology. Here we integrate environmental sequencing with biogeochemistry to interrogate patterns in abundance and community composition—as well as dispersal mechanisms and timing—that underlie microbial migration in natural ecosystems. Our analysis focuses on the presence of and similarities across high identity genomic DNA scaffolds and fragments, thousands of which are distributed across over two dozen communities sampled from hydrothermal ecosystems from Yellowstone National Park, Wyoming and Great Boiling Springs, Nevada. Results Despite their geographical isolation from one another and physico-chemical isolation from surrounding mesophilic environments, a large number (&43,000) of long, high identity DNA scaffolds were conserved across two or more hot springs communities. This widespread distribution of nearly identical DNA fragments suggests active mechanisms driving microbial migration and genomic information sharing. Genes encoded on these scaffolds encompass a broad spectrum of metabolic capabilities from diverse thermophilic taxa, but include revealing biases in the functions and taxonomic distribution of shared genes. Evolutionary rate analysis suggests that genomic migration and sharing is not only recent and ongoing, but that very different mechanisms are driving chemotrophic versus phototrophic community information exchange—mechanisms that include both biological and abiotic vectors and catastrophic events that have acted as evolutionary bottlenecks in particular on sunlight-driven photosynthetic communities. Conclusions The intersection of biology and environment is privy to an unprecedented level of interrogation as a result of advances in ecosystems biology, in particular through the integration of data from analysis across multiple scales and disciplines. Both the methodologies developed herein, and the findings our results support, help advance our understanding of microbial ecology and dispersal mechanisms in natural environments.