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

Abstract

Bloom-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.

Keywords: Alternative stable states; Co-evolution; Ecosystem engineering; HAB formation and management; Metalimnion; Niche construction; Reservoirs.

Fig. 1

Conceptual model to predict the occurrence of Planktothrix rubescens surface blooms (Walsby et al., 2004). z_m, mixing depth; z_n, depth in which filaments gain neutral buoyancy; z_q, critical depth for buoyancy (modified from Walsby et al., 2005).

Fig. 2

Map showing distribution of records of Planktothrix spp. either from isolation (polyphasic taxonomy, circles) or microscopical inspection (square symbols). Occurrence data from: Pridmore and Etheredge (1987), Baker and Humpage (1994), Kruk et al. (2002), Suda et al. (2002), Kemka et al. (2003), Bouchamma et al. (2004), Wood et al. (2005), Lin et al. (2010), Kurmayer et al. (2015).

Fig. 3

Overview of toxic and bioactive peptide structural variants representing peptide families isolated from Planktothrix (Oscillatoria).

Fig. 4

Overview of gene clusters encoding either nonribosomal peptide synthesis (NRPS), hybrid polyketide synthesis (PKS)-NRPS, or ribosomally synthesized and posttranslationally modified peptides (RiPPs) in Planktothrix agardhii and P. rubescens.

Fig. 5

(A) Relationship between MC content (μg MC-LR equiv. mg dry weight (DW)⁻¹) as determined from strains of Planktothrix agardhii and P. rubescens in the course of two consecutive experiments performed during 2003–2004 (Kosol et al., 2009) and 2009–2010 (R.K. unpublished data). (B) Schematic view of the mcy gene cluster consisting of nine genes encoding MC synthesis and nucleotide sequence variation within the intergenic spacer region as observed from 13 strains (see Table 2). The red lines indicate the loci used for quantification of the transcript amount by qPCR. (C) Average ± SE transcript amounts of mcy genes determined for low MC-producing and high MC-producing strains using rpoC as a reference (see Table 2). (D) Relationship between mcyG transcript amount and MC content per dry weight or per biovolume from strains (Table 2).

Fig. 6

(A) Scheme on inheritance of the mcy gene cluster in Planktothrix spp. according to Kurmayer et al. (2015) and unpublished data (R.K.). *Ia, Ib denote lineages according to Gaget et al. (2015). (B) Phylogenetic tree showing relatedness of Planktothrix species according to MLSA (Kurmayer et al., 2015). (C) Phylogenetic tree showing relatedness of Planktothrix species according to mcy gene cluster 5′-end flanking regions (254 bp), (R.K. unpublished).

Fig. 7

Distribution of gene loci indicative of peptide synthesis gene clusters within Planktothrix phylogenetic lineages (Kurmayer et al., 2015) (R.K., E.E., unpublished data, Supplementary Table 2).

Fig. 8

Population genetic structure as revealed by mcyBA1 restriction type profiling showing the existence of homogeneous and more heterogeneous populations in geographically close but spatially isolated lakes during several years (Kurmayer and Gumpenberger, 2006).