Role of toxic and bioactive secondary metabolites in colonization and bloom formation by filamentous cyanobacteria Planktothrix

Abstract

SummaryBloom-forming cyanobacteria Planktothrix agardhii and P. rubescens are regularly involved in the occurrence of cyanotoxin in lakes and reservoirs. Besides microcystins (MCs), which inhibit eukaryotic protein phosphatase 1 and 2A, several families of bioactive peptides are produced, thereby resulting in impressive secondary metabolite structural diversity. This review will focus on the current knowledge of the phylogeny, morphology, and ecophysiological adaptations of Planktothrix as well as the toxins and bioactive peptides produced. The relatively well studied ecophysiological adaptations (buoyancy, shade tolerance, nutrient storage capacity) can partly explain the invasiveness of this group of cyanobacteria that bloom within short periods (weeks to months). The more recent elucidation of the genetic basis of toxin and bioactive peptide synthesis paved the way for investigating its regulation both in the laboratory using cell cultures as well as under field conditions. The high frequency of several toxin and bioactive peptide synthesis genes observed within P. agardhii and P. rubescens, but not for other Planktothrix species (e.g. P. pseudagardhii), suggests a potential functional linkage between bioactive peptide production and the colonization potential and possible dominance in habitats. It is hypothesized that, through toxin and bioactive peptide production, Planktothrix act as a niche constructor at the ecosystem scale, possibly resulting in an even higher ability to monopolize resources, positive feedback loops, and resilience under stable environmental conditions. Thus, refocusing harmful algal bloom management by integrating ecological and phylogenetic factors acting on toxin and bioactive peptide synthesis gene distribution and concentrations could increase the predictability of the risks originating from Planktothrix blooms.

Cyanobacterial dynamics and toxins concentrations in Lake Alto Flumendosa, Sardinia, Italy

“…However, in this study the application of the linear regression to the mcyB + cells and MC reduced the percentage of MC variation explained, from >80% to ~50%, i.e., a value very close to what was observed by Briand et al (2008) in a population of P. agardhii and consistent with what we previously described in Lake Vico (Manganelli et al, 2016). There are several possible explanations for this outcome, as summarized in Kurmayer et al (2016), such as other coexisting non identified toxic species, problems in the amplification of mcy genes or mutation inactivating mcy genes. Or it could be also hypothesized that other factors, in addition to the genetic make up, influence the relationship between density and toxicity, and the relation between the whole population and MC, representing the environmental cell quota (ECQ, sensu Salmaso et al, 2014), includes those factors.…”

“…The strong relationship between CB and MC in P. rubescens implies a high stability of population genetic structure over time (Salmaso et al, 2014;Kurmayer et al, 2016), which is indeed what we found in the Flumendosa reservoir. But this is not always the case: in Lake Vico (Central Italy), where P. rubescens was dominant, the fraction of the mcyB + cells was highly variable over time, especially during the blooms.…”

“…The overall density of CB community during our study was about 10 times lower than what was observed before (Messineo et al, 2009;Sulis et al, 2014), but an even more complex alternation of species was observed. P. rubescens was always present and generally dominant until summer 2012, with the typical trend of depth blooms in summer and more homogeneous distribution along the water column during the other seasons (Kurmayer et al, 2016). These results confirmed the need to sample the metalimnetic layers, especially when they are the source of drinking water supply (Manganelli et al, 2010(Manganelli et al, , 2016.…”

Interspecific Relationship and Ecological Requirements of Two Potentially Harmful Cyanobacteria in a Deep South-Alpine Lake (L. Iseo, I)

“…Unlike T. bourrellyi, P. rubescens has these structures and, therefore, has an important competitive advantage. P. rubescens is able to move along the water column and consequently acquire the most favorable position [4,[63][64][65][66][67]. The physiological features and environmental factors that allow the co-presence of these two Cyanobacteria have not yet been identified.…”

“…The presence of gas vesicles in this species could allow the overcoming of the tendency of Cyanobacteria to sink out of the euphotic zone, providing P. rubescens with a competitive advantage. Changes in cellular weight due to photosynthesis and respiration processes can be balanced with gas vesicles [65,66,81]. Moreover, the buoyancy ability allows each species to optimize light absorption and obtain the most favorable positioning in the water column.…”