Incomplete Selective Sweeps of Microcystis Population Detected by the Leader-End CRISPR Fragment Analysis in a Natural Pond

Tominaga

Nishimura

et al. 2019

Appl Environ Microbiol

Self Cite

Viruses play important roles in regulating the abundance and composition of bacterial populations in aquatic ecosystems. The bloom-forming toxic cyanobacterium Microcystis aeruginosa is predicted to interact with diverse cyanoviruses, resulting in Microcystis population diversification. However, current knowledge of the genomes from these viruses and their infection programs is limited to those of Microcystis virus Ma-LMM01. Here, we performed a time series sampling at a small pond in Japan during a Microcystis bloom and then investigated the genomic information and transcriptional dynamics of Microcystis-interacting viruses using metagenomic and metatranscriptomic approaches. We identified 15 viral genomic fragments classified into three groups, groups I (including Ma-LMM01), II (high abundance and transcriptional activity), and III (new lineages). According to the phylogenetic distribution of Microcystis strains possessing spacers against each viral group, the group II-original viruses interacted with all three phylogenetically distinct Microcystis population types (phylotypes), whereas the groups I and III-original viruses interacted with only one or two phylotypes, indicating the cooccurrence of broad- (group II) and narrow (groups I and III)-host-range viruses in the bloom. These viral fragments showed the highest transcriptional levels during daytime regardless of their genomic differences. Interestingly, M. aeruginosa expressed antiviral defense genes in the environment, unlike what was seen with an Ma-LMM01 infection in a previous culture experiment. Given that broad-host-range viruses often induce antiviral responses within alternative hosts, our findings suggest that such antiviral responses might inhibit viral multiplication, mainly that of broad-host-range viruses like those in group II. IMPORTANCE The bloom-forming toxic cyanobacterium Microcystis aeruginosa is thought to have diversified its population through the interactions between host and viruses in antiviral defense systems. However, current knowledge of viral genomes and infection programs is limited to those of Microcystis virus Ma-LMM01, which was a narrow host range in which it can escape from the highly abundant host defense systems. Our metagenomic approaches unveiled the cooccurrence of narrow- and broad-host-range Microcystis viruses, which included fifteen viral genomic fragments from Microcystis blooms that were classified into three groups. Interestingly, Microcystis antiviral defense genes were expressed against viral infection in the environment, unlike what was seen in a culture experiment with Ma-LMM01. Given that viruses with a broad host range often induce antiviral responses within alternative hosts, our findings suggest that antiviral responses inhibit viral reproduction, especially that of broad-range viruses like those in group II. This paper augments our understanding of the interactions between M. aeruginosa and its viruses and fills an important knowledge gap.

Section: Discussionmentioning

confidence: 79%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Cooccurrence of Broad- and Narrow-Host-Range Viruses Infecting the Bloom-Forming Toxic Cyanobacterium Microcystis aeruginosa

Tominaga

Nishimura

et al. 2019

Appl Environ Microbiol

Self Cite

“…However, there are diverse genotypes even within a single bacterial species in the environment, as observed in metagenomic islands, which are under-represented regions among all the genomes of one bacterial species (Rodriguez-Valera et al, 2009;Rodriguez-Valera and Ussery, 2012). For example, Microcystis blooms are composed of highly diverse genotypic populations (Yoshida et al, 2005;Kuno et al, 2014;Yang et al, 2015;Kimura et al, 2018). Thus, recent understanding of the virus-host coexistence relies on the concept of multiple genotype (strain)-level interactions at the species or population level (Thingstad et al, 2015), which encompass a range from highly resistant to susceptible host cells and from broad and narrow host range cyanoviruses (Morimoto et al, 2019).…”

Section: Competitive Evolution Between Cyanoviruses and Freshwater Blmentioning

confidence: 99%

“…The coexistence of diverse host genotypes within the population can be established by the viral infection of the dominant host genotype (Thingstad et al, 2014(Thingstad et al, , 2015. The ecological consequences of such viral control have been intensively studied in M. aeruginosa and indicated that multiple Microcystis populations possessing different CRISPR arrays exist in their massive blooms (Kuno et al, 2012(Kuno et al, , 2014 and oscillate in the environment (Kimura et al, 2018). Such continuous interactions have also been predicted between A. flos-aquae and its cyanovirus vB_AphaS-CL131 (Šulčius et al, 2019).…”

Section: Competitive Evolution Between Cyanoviruses and Freshwater Blmentioning

confidence: 99%

Viruses of freshwater bloom‐forming cyanobacteria: genomic features, infection strategies and coexistence with the host

Šulčius²,

Yoshida

2020

Environ Microbiol Rep

Self Cite

Summary Freshwater bloom‐forming cyanobacteria densely grow in the aquatic environments, leading to an increase in the viral‐contact rate. They possess numerous antiviral genes, as well as cell differentiation‐ and physiological performance‐related genes, owing to genome expansion. Their genomic features and unique lifestyles suggest that they coexist with cyanoviruses in ways different from marine cyanobacteria. Furthermore, genome contents of isolated freshwater bloom‐forming cyanobacterial viruses have little in common with those of marine cyanoviruses studied to date. They lack the marine cyanoviral hallmark genes that sustain photosynthetic activity and redirect host metabolism to viral reproduction; therefore, they are predicted to share metabolisms and precursor pools with host cyanobacteria to ensure efficient viral reproduction and avoid nutrient deficiencies and antiviral response. Additionally, cyanovirus–cyanobacteria coexistence strategies may change as bloom density increases. Diverse genotypic populations of cyanoviruses and hosts coexist and fluctuate under high viral‐contact rate conditions, leading to their rapid coevolution through antiviral responses. The ancestral and newly evolved genotypes coexist, thereby expanding the diversity levels of host and viral populations. Bottleneck events occurring due to season‐related decreases in bloom‐forming species abundance provide each genotype within cyanobacterial population an equal chance to increase in prevalence during the next bloom and enhance further diversification.

Viral Nature of the Aquatic Ecosystems

The Biological Role of a Virus

Tominaga

Takebe

et al. 2022

Self Cite

Viruses infecting microorganisms are ubiquitous and highly abundant in aquatic environments. They considerably affect the dynamics, diversity, and evolution of their host microorganisms. In this review, we discuss the ecological implications of viruses from the perspectives of the biogeochemical cycles, microbial diversity, and virus-host coevolutionary dynamics in aquatic environments. Generally, viruses redirect host metabolism toward reproduction through molecular host-virus interactions characterized by the compositional and stoichiometric changes in intracellular metabolites, which are eventually released into the environment when the infected host cells are lysed, thus also changing the chemical composition of the water. Therefore, the modulation of metabolite biosynthesis and promotion of their recycling are major viral functions. Viruses also maintain microbial community diversity via increased infection and lysis rates of the dominant taxa and genotypes in a frequency-dependent manner, thereby allowing the co-existence of members with various competitive abilities. Finally, viruses can expand their own genotypic diversity and that of the host through complex defense and counter-defense interactions, including loss of host fitness due to the cost of resistance and the possible need for antiviral defense-specific (e.g., intra-vs. extracellular) changes in the hosts genome diversification. Continuous interactions drive 3 the coevolution of hosts and viruses, thereby increasing both the host and viral micro-diversity. Hence, these fundamental functions are viral "raison d'etre" and are essential for the functioning of aquatic ecosystems and its components.