Tracking Microcystis viruses and infection dynamics across distinct phases of a Microcystis-dominated bloom

Abstract

Given the impact of viruses on microbial community composition and function, viruses have the potential to play a significant role in the fate of freshwater cyanobacterial harmful algal blooms (cHABs). Yet the role of viruses in cHABs remains poorly understood. We sought to address this knowledge gap with a metagenomic analysis of viruses of bloom-forming Microcystis aeruginosa across cHAB phases in the western basin of Lake Erie. Size-fractionation of the water allowed us to identify significant fraction-specific trends in viral diversity, which corresponded with Microcystis genetic diversity. Using a new machine-learning model, we predicted infections between viral and microbial host populations. We predicted hundreds of viral populations with infection histories including Microcystis and non-Microcystis hosts, suggesting extensive interconnectivity and the potential for virus-mediated cross-species exchange of genetic material within cHABs communities. Infection predictions revealed a broad host range for Lake Erie Microcystis viruses, challenging previous notions of "narrow" host-virus interactions in cHABs. Abundant viral genes belonging to predicted Microcystis viruses revealed their potential role in key metabolic pathways and adaptation to environmental changes. We observed significant turnover of predicted Microcystis virus populations across time. Viral diversity was highest in the viral fraction and lowest in the colony-associated fraction, suggesting that Microcystis colony formation and growth during cHABs leads to bottlenecks in viral diversity. These findings advance our understanding of uncultivated Microcystis virus diversity, their potential effects on host metabolism, potential influence on species interactions, and potential coevolutionary processes between microbial hosts and their viral predators within Microcystis-dominated cHABs. ImportanceUnderstanding interactions between viruses, their hosts, and environmental parameters may be key to identifying the mechanisms underlying the persistence and demise of cyanobacterial harmful algal blooms (cHABs). In this study we describe the viral diversity and host ranges of viruses predicted to infect Microcystis, describing the distribution of these properties across time, space, and different bloom-associated size fractions. Additionally, the study highlights abundant genes belonging to predicted Microcystis viruses and their potential roles in key metabolic pathways and adaptation to environmental changes. The observed turnover of Microcystis virus populations, with the highest diversity in viral fractions and the lowest in colony-associated fractions, suggests that Microcystis colony formation during blooms plays an important role in shaping viral diversity and community turnover. These findings contribute to a better understanding of the interplay between viruses, Microcystis, and their accompanying bacterial communities, shedding light on mechanisms driving bloom dynamics, species interactions, and coevolutionary processes.