Temporal Dynamics of Cyanobacterial Bloom Community Composition and Toxin Production from Urban Lakes

Abstract

With a long evolutionary history and a need to adapt to a changing environment, cyanobacteria in freshwater systems use specialized metabolites for communication, defense, and physiological processes. Furthermore, many cyanobacterial specialized metabolites and toxins present significant human health concerns due to their liver toxicity and their potential impact to drinking water. Gaps in knowledge exist with respect to changes in species diversity and toxin production during a cyanobacterial bloom (cyanoHAB) event; addressing these gaps will improve understanding of impacts to public and ecological health. In the current report we detail community and toxin composition dynamics during a late bloom period. Species diversity decreased at all study sites over the course of the bloom event, and toxin production reached a maximum at the midpoint of the event. We also isolated three new microcystins from a Microcystis dominated bloom (1-3), two of which contained unusual doubly homologated tyrosine residues (1 and 2). This work provokes intriguing questions with respect to the use of allelopathy by organisms in these systems and the presence of emerging toxic compounds that can impact public health.

Keywords: DNA metabarcoding; cyanobacteria; harmful algal blooms; microcystins; molecular networking.

Figure 1.

(A) CyanoHAB community composition and successional patterns. Relative abundances of cyanobacterial taxa at Cunliff, Pleasure, and Polo Lakes from 9/1/2022 to 12/7/2022. (B) NMDS plots of the cyanobacterial taxa composition at all sites for early and late bloom periods. There was significant difference observed in the similarity of community composition in the two periods (ANOSIM, p < 0.001, R = 0.586).

Figure 2.

Species diversity decreased over the course of cyanoHABs. Alpha diversity measurement of individual discrete samples from field sites completed over the time period 9/1/2022 to 12/7/2022 determined by Chao and Shannon metrics.

Figure 3.

Cyanotoxin annotation and relative concentration at Pleasure, Cunliff, and Polo Lakes during the study period from 9/1/2022 to 12/7/2022. The colors in the heat maps are proportional to the intensity of the extracted ion for each analyte. Precursor masses for each toxin are listed in the parentheses.

Figure 4.

LC-MS/MS network of all extracts from surface water samples during the study period. Nodes are designated by their precursor m/z values (e.g., 995.616 is the precursor m/z value for microcystin-LR) and grouped into toxin classes. Pie slices indicate in which lake metabolites were detected (Pleasure, green; Cunliff, yellow; Polo, purple). Hexagons indicate that metabolites were amongst the 14 annotated in the study, while parallelograms indicate metabolites that are putatively known but were not specifically monitored. Squares indicate putatively new toxins.

Figure 5.

PCA analysis of bloom metabolites. (A) Comparison by site showed similarities in metabolite profiles among all sites. Asterisks show outliers (top to bottom: Pleasure 11/2/2022; Pleasure 11/9/2022; Cunliff 11/9/2022; Pleasure 11/30/2022. (B) Separating by early and late bloom periods showed differences in metabolite profiles.

Figure 6.

Structures of compounds 1–3.