Viral Impacts on Total Abundance and Clonal Composition of the Harmful Bloom-Forming Phytoplankton Heterosigma akashiwo

Abstract

Recent observations that viruses are very abundant and biologically active components in marine ecosystems suggest that they probably influence various biogeochemical and ecological processes. In this study, the population dynamics of the harmful bloom-forming phytoplankton Heterosigma akashiwo (Raphidophyceae) and the infectious H. akashiwo viruses (HaV) were monitored in Hiroshima Bay, Japan, from May to July 1998. Concurrently, a number of H. akashiwo and HaV clones were isolated, and their virus susceptibilities and host ranges were determined through laboratory cross-reactivity tests. A sudden decrease in cell density of H. akashiwo was accompanied by a drastic increase in the abundance of HaV, suggesting that viruses contributed greatly to the disintegration of the H. akashiwo bloom as mortality agents. Despite the large quantity of infectious HaV, however, a significant proportion of H. akashiwo cells survived after the bloom disintegration. The viral susceptibility of H. akashiwo isolates demonstrated that the majority of these surviving cells were resistant to most of the HaV clones, whereas resistant cells were a minor component during the bloom period. Moreover, these resistant cells were displaced by susceptible cells, presumably due to viral infection. These results demonstrated that the properties of dominant cells within the H. akashiwo population change during the period when a bloom is terminated by viral infection, suggesting that viruses also play an important role in determining the clonal composition and maintaining the clonal diversity of H. akashiwo populations. Therefore, our data indicate that viral infection influences the total abundance and the clonal composition of one host algal species, suggesting that viruses are an important component in quantitatively and qualitatively controlling phytoplankton populations in natural marine environments.Viruses are now recognized as the most abundant and biologically active components of marine ecosystems (1, 24). Field studies indicate that the majority are probably bacterial viruses, i.e., bacteriophages (5, 33), but viruses and viruslike particles have been observed in many phytoplankton species and in a wide range of natural seawater samples (8,28,32). These observations have led to increased interest in the impact of viral infection on the population dynamics and community structure of marine phytoplankton. Several studies have suggested that viruses can be significant agents of phytoplankton mortality. For example, an addition of native virus concentrates reduced phytoplankton biomass and primary productivity under experimental laboratory conditions (28, 29). Also, electron microscopic observations have shown that the proportion of cells harboring viruslike particles or the abundance of viruslike particles within the water column increases in the final stages of blooms (2,3,16,17). In contrast to these postulates, a few reports have demonstrated that viruses are probably not responsible for a large proportion of host mortality (33,36). Wat...

Effects of solar ultraviolet radiation on photosynthesis of the marine red tide alga Heterosigma akashiwo (Raphidophyceae)

“…At the same time, it had been shown allelopathic effects towards other algae, specifically diatoms [30]. The growth and toxicity of H. akashiwo can be mediated by hydrogen peroxide [24,31] or viruses [32,33]. In addition, and more relevant to the blooms H. akashiwo in a climate change environment, [34] showed that growth and toxicity of this alga was markedly influenced by changes in temperature and light intensity.…”

Viral lysis of Phaeocystis pouchetii: Implications for algal population dynamics and heterotrophic C, N and P cycling

“…The potential influence of viruses on phytoplankton mortality and population dynamics is well known for marine environments (for example, Bratbak et al, 1993Bratbak et al, , 1995Brussaard et al, 1996bBrussaard et al, , 2007, as verified by demonstrations of virus-induced termination of algal blooms (for example, Bratbak et al, 1993;Tarutani et al, 2000;Castberg et al, 2001;Brussaard et al, 2005b), and the potential of viruses as controlling agents for keeping algal populations at non-blooming levels (for example, Zingone et al, 1999;Larsen et al, 2001;Brussaard et al, 2005b).…”

“…Resistance to viral infection has also been demonstrated in populations of cyanobacteria. (Waterbury and Valois, 1993;Suttle and Chan, 1994;Lennon et al, 2007), as well as in eukaryotic algae (Tarutani et al, 2000;Jacquet et al, 2002;Schroeder et al, 2003;Thyrhaug et al, 2003). For Phaeocystis, the morphology of the cells (solitary vs colonial) has been shown to influence susceptibility to viral control, with single cells being much more vulnerable to viral infection than colonial cells (Brussaard et al, 2007).…”

Seasonal determinations of algal virus decay rates reveal overwintering in a temperate freshwater pond

“…Their high abundance and obligately parasitic lifestyle allow viruses to exert top-down control of cellular organism populations, which is illustrated most dramatically through the implication that viruses are involved in the termination of some algal blooms (e.g., Bratbak et al, 1993;Tarutani et al, 2000;Wilson et al, 2002;Brussaard et al, 2005: Gobler et al, 2007Tomaru et al, 2007). More subtly, viruses contribute to the mortality of bacteria, phytoplankton and higher trophic levels of the aquatic food web (Proctor and Fuhrman, 1990;Suttle, 1994;Baudoux et al, 2006).…”