Ecological Dynamics of the Toxic Bloom-Forming Cyanobacterium Microcystis aeruginosa and Its Cyanophages in Freshwater

Abstract

The abundance of potentially Microcystis aeruginosa-infectious cyanophages in freshwater was studied using g91 real-time PCR. A clear increase in cyanophage abundance was observed when M. aeruginosa numbers declined, showing that these factors were significantly negatively correlated. Furthermore, our data suggested that cyanophage dynamics may also affect shifts in microcystin-producing and non-microcystin-producing populations.The major bloom-forming cyanobacterial species Microcystis aeruginosa forms noxious blooms in many eutrophic freshwater lakes, ponds, and reservoirs. A limited population (limited number of strains) of M. aeruginosa in the environment produces potent hepatotoxins called microcystins (7). These potent toxins in the M. aeruginosa blooms have caused many cases of animal and human poisoning (3,8,16).Previously, most studies have focused on relationships among the cyanobacterial bloom dynamics and the changes in physicochemical factors (e.g., nutrient supply, light, and temperature) that influence cyanobacterial growth in the aquatic environment (28). Since the discovery that viruses are widespread in marine ecosystems (4), cyanophages that can infect cyanobacteria have been thought to be an alternative factor that may control the succession of cyanobacterial blooms (12,14,15,18,19). In addition, cyanophages can also influence the clonal composition of the host Synechococcus communities (14, 27) and could account for some of the cyanobacterial diversity observed in natural communities (22,25,30). Nevertheless, little is known about how freshwater cyanophages can affect the abundance and clonal composition of cyanobacterial blooms in lakes over time.Our aim is to determine if the cyanophages have potential quantitative and qualitative effects on the M. aeruginosa communities in Lake Mikata in Japan. We performed two independent real-time PCR assays to monitor the dynamics of M. aeruginosa and its cyanophage communities. To quantify M. aeruginosa, we used the phycocyanin intergenic spacer (PC-IGS) that was previously used to examine total M. aeruginosa numbers (9, 32). A second real-time PCR assay was used to quantitatively detect potentially M. aeruginosa-infectious cyanophages using the primers targeting the viral sheath proteinencoding gene (g91) previously identified by Takashima et al.(21). To determine the effect of the cyanophages on the internal dynamics of the total M. aeruginosa communities, we examined the fluctuation in the abundance of potentially microcystin-producing M. aeruginosa populations using the real-time PCR and microcystin synthetase gene (mcyA)-specific primers (32) and monitored the relative size of the microcystin-producing subpopulation compared to the total population in relation to the cyanophage numbers using a field survey of M. aeruginosa blooms in a Japanese lake.Water samples were collected from the surface layer (0.5 m) once per month from April to October in 2006 at a fixed point (35°33ЈN, 135°53ЈE) in Lake Mikata (Fig. 1). The cyanobacterial cells used for ...

Dynamics of the water bloom-forming Microcystis and its relationship with physicochemical factors in Lake Xuanwu (China)

“…Cell numbers of Microcystis detected by the qPCR analysis were found to be 1-30 times higher than those by microscopic examination, which is consistent with results of several previous studies (Vaitomaa et al 2003;Hotto et al 2007;Yoshida et al 2008). Lower values of cell abundance examined by the microscopic counting method, especially for Microcystis and cyanobacteria that occur in late winter and early spring having low numbers, may result from the low detection limit, colonial decomposition, and cell loss during the longer fixation procedure by the microscopic counting approach (Hotto et al 2007).…”

“…It is generally known that cyanobacterial blooms, dominated by either Microcystis or Planktothrix, consist of both toxic and nontoxic populations (Kurmayer et al 2002(Kurmayer et al , 2004Yoshida et al 2008). Several recent studies using qPCR or competitive PCR to amplify fragments of the mcy gene involved in MC production have revealed that proportions of mcy-containing Microcystis were relatively low, i.e., 1-38% for mcyB subpopulations in Lake Wannsee, Germany, 0.5-35% for mcyA subpopulations in Lake Mikata, Japan, 0-37% for mcyD subpopulations in Lake Oneida, USA, and 0-48% for mcyD subpopulations in Lake Erie, respectively (Kurmayer and Kutzenberger 2003;Yoshida et al 2007;Hotto et al 2008;Rinta-Kanto et al 2009).…”

Trade-Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the “Killing the Winner” Hypothesis Revisited

“…In accordance with KtW, a number of studies in marine and freshwater environments found that virus and host communities of either specific populations or entire assemblages are linked (26,37,33,51,69,96,98,107,108,112), and there is evidence suggesting similarly coupled prokaryotic and viral communities in a soda lake (80). The details vary, however.…”

“…In agreement with KtW, those authors' results show that viruses were closely linked to the developments in the microbial community. Also, Wang and Chen (98) investigated the population dynamics of cyanovirus communities, and Yoshida et al (112) studied the dynamics of viruses infecting the toxic bloom-forming cyanobacterium Microcystis aeruginosa. Both studies found that changes in the virus communities were related to changes in the host communities, supporting KtW.…”

Unraveling the genome structure of cyanobacterial podovirus A-4L with long direct terminal repeats

“…Cyanobacterial viruses, termed "cyanophages," are also abundant in both marine and freshwater ecosystems and play an important role in regulating the cyanobacteria biomass and community structure, controlling the cyanobacteria bloom, mediating the horizontal gene transfer between cyanobacterial hosts and maintaining the extensive diversity of microbial communities (Lindell et al, 2004;Sullivan et al, 2005;Yoshida et al, 2008;Gao et al, 2009;Zhang and Gui, 2012;Li et al, 2013;Ou et al, 2013;Zhang, 2014). As a preface to gain insight into the biological properties of cyanophages and their interactions with cyanobacterial hosts at the molecular level, it is necessary to obtain their complete genome sequences.…”