The eco-evolutionary dynamics of microbial populations

Thesis: Ph. D. in Microbiology Graduate Program, Massachusetts Institute of Technology, Department of Biology, 2019Cataloged from PDF version of thesis.Includes bibliographical references.Microbes have adapted to life in complex microbial communities in a large variety of ways, and they are continually evolving to better compete in their changing environments. But identifying the conditions that a particular microbe thrives under, and how they have become adapted to those condition can be exceedingly difficult. For instance, Clostridium difficile became widely known for being the world's leading cause of hospital associated diarrhea, but people can also have C. difficile in their gut without developing diarrhea. Although these asymptomatic carriers are now thought to be the largest source of infection, we know very little about how these people become colonized. In the first chapter of my thesis I use publicly available microbiome survey data and a mouse model of colonization to show that C. difficile colonizes people immediately after diarrheal illnesses, suggesting C. difficile is a disturbance adapted opportunist.However, the differences between very recently diverged microbial populations that are adapted for growth in different conditions can be very difficult to detect. To address this limitation, I developed a method of identifying regions that have undergone recent selective sweeps in these populations as a means of distinguishing them, and specifically quantifying their abundance in complex environments. But part of what makes microbial evolution so difficult to interpret is the vast diversity of genes that are only shared by a fraction of all the members in a population. To better understand how these flexible regions are structured, I systematically extracted all contiguous flexible regions in nine marine Vibrio populations and compared their organization and evolutionary histories.I found that horizontal gene transfer and social interactions have led to the evolution of modular gene clusters that mediate forms of social cooperation, metabolic tradeoffs, and make up a substantial portion of these flexible genomic regions. The observations made in these studies help us understand how microbes are organized into socially and ecologically cohesive groups, and how they have evolved to interact with complex and changing environments.by David VanInsberghe.Ph. D. in Microbiology Graduate ProgramPh.D.inMicrobiologyGraduateProgram Massachusetts Institute of Technology, Department of Biolog

How can microbial population genomics inform community ecology?

Populations are fundamental units of ecology and evolution, but can we define them for bacteria and archaea in a biologically meaningful way? Here, we review why population structure is difficult to recognize in microbes and how recent advances in measuring contemporary gene flow allow us to identify clearly delineated populations among collections of closely related genomes. Such structure can arise from preferential gene flow caused by coexistence and genetic similarity, defining populations based on biological mechanisms. We show that such gene flow units are sufficiently genetically isolated for specific adaptations to spread, making them also ecological units that are differentially adapted compared to their closest relatives. We discuss the implications of these observations for measuring bacterial and archaeal diversity in the environment. We show that operational taxonomic units defined by 16S rRNA gene sequencing have woefully poor resolution for ecologically defined populations and propose monophyletic clusters of nearly identical ribosomal protein genes as an alternative measure for population mapping in community ecological studies employing metagenomics. These population-based approaches have the potential to provide much-needed clarity in interpreting the vast microbial diversity in human and environmental microbiomes. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.National Science Foundation (Grant NSF1831730

Viruses of the Nahant Collection, characterization of 251 marine Vibrionaceae viruses

Viruses are highly discriminating in their interactions with host cells and are thought to play a major role in maintaining diversity of environmental microbes. However, large-scale ecological and genomic studies of co-occurring virus-host pairs, required to characterize the mechanistic and genomic foundations of virus-host interactions, are lacking. Here, we present the largest dataset of cultivated and sequenced co-occurring virus-host pairs that captures ecologically representative fine-scale diversity. Using the ubiquitous and ecologically diverse marine Vibrionaceae as a host platform, we isolate and sequence 251 dsDNA viruses and their hosts from three time points within a 93-day time-series study. The virus collection includes representatives of the three Caudovirales tailed virus morphotypes, a novel family of nontailed viruses, and the smallest (10,046 bp) and largest (348,911 bp) Vibrio virus genomes described. We provide general characterization and annotation of the viruses and describe read-mapping protocols to standardize genome presentation. The rich ecological and genomic contextualization of hosts and viruses make the Nahant Collection a unique platform for high-resolution studies of environmental virus-host infection networks.National Science Foundation (U.S.) (OCE 1435993