Dynamics of microcystin-degrading bacteria in mucilage of Microcystis

Abstract

To reveal the process of degradation of hepatotoxic microcystin produced in Microcystis cells during the Microcystis bloom period, we used fluorescence in situ hybridization (FISH) to analyze the population dynamics of microcystin-degrading bacteria in Microcystis mucilage. We designed and applied an oligonucleotide probe targeted to the 16S rRNA sequence of strain Y2 of a microcystin-degrading bacterium (MCD-bacterium), which was isolated from Lake Suwa, Japan. In both the 1998 and 1999 tests, FISH clearly showed that MCD-bacteria existed in the mucilage and that, when a high concentration of cell-bound microcystin was detected, MCD-bacteria exceeded 10% of the sum of bacteria hybridized with group-specific probes. The concentration of MCD-bacteria was highest in summer 1998, when a toxic species, M. viridis, was dominant. There was a high correlation between the number of MCD-bacteria in the mucilage and the concentration of cell-bound microcystin in the lake. Our results suggest that MCD-bacteria responded to changes in the concentration of microcystin and degraded the microcystin when it was released from Microcystis cells. We also analyzed changes in the bacterial community structure associated with the Microcystis colonies by using domain- and group-specific oligonucleotide probes. Changes in the concentrations of the Cytophaga/Flavobacterium group and delta-Proteobacteria, which can degrade macromolecules derived from Microcystis cells, were synchronized with changes in the concentration of Microcystis. The results not only suggest the significant role of MCD-bacteria in detoxification, but also demonstrate a possible sequence of degradation from Microcystis cells to microcystin maintained in the cell, which is then carried out by bacterial consortia in the mucilage.

Microcystin-degrading bacteria affect mcyD expression and microcystin synthesis in Microcystis spp.

“…Mucilage has also been proved to be a habitat for bacteria that exert their specific function to utilize substrate and nutrients from decaying Microcystis cells. Maruyama et al (2003) found that MCDB existed in a limited area of the mucilage of Microcystis, so that the concentration dynamics of these bacteria were synchronized with increases in the concentration of cell-bound MC. This suggests that MCDB in the mucilage respond to changes in the concentration of cell-bound MC.…”

“…The main difference between colony and unicellular Microcystis is in the mucilage that always surrounds Microcystis (Maruyama et al, 2003). Wu and Song (2008) found that colony Microcystis usually had higher levels of EPS and polysaccharide content in the mucilage than unicellular Microcystis.…”

The Contribution of Attached Bacteria to Microcystis Bloom: Evidence From Field Investigation and Microcosm Experiment

“…The relative abundance of particle-attached Bacteroidetes, Alphaproteobacteria, and Betaproteobacteria was significant increased in general from day 0 to days 2 and 14 following the decomposition of Microcystis blooms. The reason may be related to their ability in degrade not only complex organic macromolecules (Kirchman, 2002), but also Microcystis cells (Eiler et al, 2006;Maruyama et al, 2003;Yamamoto et al, 1993). First, previous findings have highlighted the importance of Bacteroidetes, during cyanobacterial blooms (Eiler and Bertilsson, 2004), and they are able to degrade not only macromolecular compounds (Cottrell and Kirchman, 2000;Van Hatmen et al, 1999), but also Microcystis cells (Yamamoto et al, 1993).…”

“…The attached bacteria are important in the trophic dynamics of aquatic food webs and in the remineralization of dissolved and particulate organic matter (Tang et al, 2009), and understanding the response of the particle-attached bacterial community composition (PABCC) to decomposition of Microcystis blooms is very important for a better understanding of the metabolic processes in eutrophic aquatic ecosystems. Meanwhile, the interactions of algae with bacteria are diverse and complex, and have a key impact on the occurrence or duration of the algae bloom (Grossart et al, 2005(Grossart et al, , 2006Maruyama et al, 2003). Therefore, understanding changes of the taxa composition of attached bacteria during the decomposition of Microcystis blooms is crucial for determining the ecological consequences of Microcystis blooms in freshwater lakes.…”

In situ bacterial mitigation of the toxic cyanobacterium Microcystis aeruginosa: implications for biological bloom control

“…Kim et al (2007) demonstrated that the release of d-MC from Microcystis following cell lysis by algicidal bacteria could suppress growth of the anti-algal bacteria. Although a detoxification role for microcystin-degrading bacteria residing in the outer mucilage of Microcystis has been proposed (Rashidan and Bird 2001;Maruyama et al 2003), the bacteriolytic activity of M. aeruginosa via MC derivatives has not been tested in situ. Therefore, we hypothesize that the low growth or biomass of X. autotrophicus SM02 was due to unfavorable growth conditions (e.g., water temperature that was too low or too high).…”