Interplay between the genetic clades of Micromonas and their viruses in the Western English Channel

Abstract

The genus Micromonas comprises distinct genetic clades that commonly dominate eukaryotic phytoplankton community from polar to tropical waters. This phytoplankter is also recurrently infected by abundant and genetically diverse prasinoviruses. Here we report on the interplay between prasinoviruses and Micromonas with regard to the genetic diversity of this host. For 1 year, we monitored the abundance of three clades of Micromonas and their viruses in the Western English Channel, both in the environment using clade-specific probes and flow cytometry, and in the laboratory using clonal strains of Micromonas clades to assay for their viruses by plaque-forming units. We showed that the seasonal fluctuations of Micromonas clades were closely mirrored by the abundance of their corresponding viruses, indicating that the members of Micromonas genus are susceptible to viral infection, regardless of their genetic affiliation. The characterization of 45 viral isolates revealed that Micromonas clades are attacked by specific virus populations, which exhibit distinctive clade specificity, life strategies and genetic diversity. However, some viruses can also cross-infect different host clades, suggesting a mechanism of horizontal gene transfer within the Micromonas genus. This study provides novel insights into the impact of viral infection for the ecology and evolution of the prominent phytoplankter Micromonas.

Temperature is a key factor in Micromonas–virus interactions

“…Under these growth conditions, MicV-B readily adsorbed on host membranes and rapidly hijacked host cellular machinery for viral DNA replication as well as virion protein synthesis and assembly, as indicated by the short latent period (o3 h), the high burst size (140 virions per infected cell) and the fast viral production rate (5.5 day − 1 ). The observed viral parameters fall within the range of reported values for other Micromonas viral isolates (Mayer and Taylor, 1979;Baudoux and Brussaard, 2008;Baudoux et al, 2015). Decrease in temperature led to increased latent periods and the coldest temperatures (12.5 and 9.5°C) also induced a reduction of viral production rates and a substantial delay in host cell lysis.…”

“…At temperatures lower than T opt , MicV-B propagated and killed their hosts through cell lysis as classically reported in the literature (Mayer and Taylor, 1979;Zingone et al, 2006;Baudoux et al, 2015;Martínez-Martínez et al, 2015). Yet the kinetics and the intensity of viral replication slowed down with decreasing temperatures.…”

“…Viral strains RCC4253, RCC4265 and RCC4229 (hereafter referred to as MicV-A, MicV-B and MicV-C) that are lytic to Micromonas Mic-A, Mic-B and Mic-C, respectively, were chosen based on the characterization conducted in Baudoux et al (2015) ( Table 1). Viral lysates were produced by infecting host cultures grown at 20°C.…”

“…Members of this prominent genus are distributed in three discrete genetic clades (Guillou et al, 2004;Foulon et al, 2008) that are all susceptible to viral infection (Baudoux et al, 2015;Martínez-Martínez et al, 2015). Previous studies demonstrated that Micromonas viruses (MicVs) are ubiquitous, highly dynamic and induce substantial mortality through cell lysis events in natural and cultured populations Suttle, 1991, 1995;Sahlsten, 1998;Zingone et al, 1999;Evans et al, 2003;Baudoux et al, 2015).…”

“…Members of this prominent genus are distributed in three discrete genetic clades (Guillou et al, 2004;Foulon et al, 2008) that are all susceptible to viral infection (Baudoux et al, 2015;Martínez-Martínez et al, 2015). Previous studies demonstrated that Micromonas viruses (MicVs) are ubiquitous, highly dynamic and induce substantial mortality through cell lysis events in natural and cultured populations Suttle, 1991, 1995;Sahlsten, 1998;Zingone et al, 1999;Evans et al, 2003;Baudoux et al, 2015). The majority of known MicVs are lytic dsDNA viruses affiliated to the Phycodnaviridae family and the genus Prasinovirus (Mayer and Taylor, 1979;Cottrell and Suttle, 1991;Zingone et al, 2006;Martínez-Martínez et al, 2015), which may represent the most abundant viruses of eukaryotic marine plankton (Hingamp et al, 2013;Yau et al, 2015).…”