Unraveling the Eco-Evolutionary Complexity of Uncultivated Bacteriophages in the Biosphere

Abstract

Bacteriophages, or phages, have historically been distinguished by their small sizes and relatively simple genomes compared to cellular life. Discoveries over recent decades, however, have uncovered remarkably large phages, called jumbo phages, which are defined by having genomes over 200 kilobases and contain virion sizes comparable to small bacteria. These exceptionally large phages prompt questions on how such complexity emerges and persists in the virosphere, when being simple is so successful with shorter replication times and larger burst sizes. This dissertation aims to address these knowledge gaps by examining the evolutionary and ecological contexts of genomic and community-level complexity of phages using a variety of metagenomic datasets, namely from marine environments. Toward understanding the coexistence of jumbo phages among smaller phages, Chapter 1 provides a literature review on jumbo phage diversity, associated fitness tradeoffs of largeness, and predictions on which environments or ecological conditions may be enriched in jumbo phages. Chapter 2 assesses the evolutionary context giving rise to complex phages, by examining a group of phages that encode a multi-subunit DNA-dependent RNA polymerase homologous to that of cells. This gene fortuitously enabled phylogenetic analyses of phages with cellular life and revealed that these phages likely emerged prior to the divergence of bacteria and archaea, rather than acquiring the gene from their hosts more recently. Chapter 3 examines the biogeography of genomic complexity in the ocean by identifying and comparing groups of jumbo phages in seawater metagenomes of the global ocean. This work revealed that jumbo phages with distinct replication machinery also have distinct distributions, with some groups more common in surface waters than deeper waters and vice versa. Chapter 4 compares drivers of phage complexity at the community level (based on diversity) with the drivers of prokaryotic community diversity by examining seawater metagenomes from contrasting ecosystems off the coasts of the Isthmus of Panama. Despite phages' requiring their hosts to replicate, the results show that factors increasing phage and prokaryotic diversity do not always align. This discrepancy highlights the role the environment also plays in governing virus-host interactions, such as impacting dispersal ranges and adsorption efficiency. Collectively, this dissertation addresses how, what, and where complexity in the virosphere occurs using culture-independent methods and contributes to our growing understanding of the breadth of viral diversity and ecology.