Cyanobacterial blooms contribute to the diversity of antibiotic-resistance genes in aquatic ecosystems

Abstract

Cyanobacterial blooms are a global ecological problem that directly threatens human health and crop safety. Cyanobacteria have toxic effects on aquatic microorganisms, which could drive the selection for resistance genes. The effect of cyanobacterial blooms on the dispersal and abundance of antibiotic-resistance genes (ARGs) of concern to human health remains poorly known. We herein investigated the effect of cyanobacterial blooms on ARG composition in Lake Taihu, China. The numbers and relative abundances of total ARGs increased obviously during a Planktothrix bloom. More pathogenic microorganisms were present during this bloom than during a Planktothrix bloom or during the non-bloom period. Microcosmic experiments using additional aquatic ecosystems (an urban river and Lake West) found that a coculture of Microcystis aeruginosa and Planktothrix agardhii increased the richness of the bacterial community, because its phycosphere provided a richer microniche for bacterial colonization and growth. Antibiotic-resistance bacteria were naturally in a rich position, successfully increasing the momentum for the emergence and spread of ARGs. These results demonstrate that cyanobacterial blooms are a crucial driver of ARG diffusion and enrichment in freshwater, thus providing a reference for the ecology and evolution of ARGs and ARBs and for better assessing and managing water quality.

Fig. 1. Bacterial and antibiotic resistance genes (ARGs) composition in different stages of cyanobacteria blooms in Lake Taihu.

Satellite map of the three sampling sites (generated by Google Maps) and the relative abundances of the ten most common genera in the bacterial community in each sampling month and site (a). ARG classifications based on antibiotic resistance mechanisms (b) and the antibiotic classes to which they confer resistance (c). Abundances and numbers of ARGs associated with various antibiotics and MGEs during the cyanobacterial blooms (n = 4) in Lake Taihu (d).

Fig. 2. Relationships between ARGs and bacterial communities in Lake Taihu.

An RDA analysis was used to determine the correlations among the abundances of ARGs, bacteria, cyanobacteria, and MGEs. The ARGs of different samples are represented by dots with different colors, and bacteria, cyanobacteria and MGEs are represented by arrows and the inner panel shows the correlations among bacteria and MGEs (a). Bray−Curtis similarity of the bacterial communities and ARG compositions between each sampling month (b). **indicates significant differences between the bacterial communities and ARG compositions at P < 0.01 by a one-way ANOVA, and n.s. indicates not significant. Network analysis identifying the patterns of co-occurrence among the ARGs, MGEs and bacteria (top 10 genera) with significant correlations (c). The size and color of the nodes represent the linking numbers of patterns and the classes of the ARGs, MGEs and bacteria, respectively. The width of the line represents the strength of the correlation. Only strong (Pearson, r > 0.6) and significant (P < 0.05) correlations are shown.

Fig. 3. Composition and diversity of ARGs in the different co-culture systems, including the urban river and Lake West cocultured with Microcystis aeruginosa (+Ma) and Planktothrix agardhii (+Pa).

Principal coordinate analysis (PCoA) of ARG communities in an urban river (a) and Lake West (b) using Bray−Curtis distances. The numbers of detected ARGs in urban river (c) and Lake West (d). The absolute abundances of ARGs in urban river (e) and Lake West (f) and relative abundances of various types of ARGs in urban river (g) and Lake West (h). Different letters indicate significant differences between the control and treatments (P < 0.05, one-way ANOVA). Data from four replicates (n = 4) are represented as means ± SD.

Fig. 4. Diversities of bacterial communities and correlations between ARG abundance and the bacterial communities.

Alpha diversities (Sob, Shannon, and Ace indices) of bacterial communities in the co-culture systems, including the urban river and Lake West co-cultured with Microcystis aeruginosa (+Ma) and Planktothrix agardhii (+Pa) (a). Principal coordinate analysis (PCoA) of bacterial communities in urban river and Lake West using weighted Unifrac distances (b). Correlations between ARG abundance and the bacterial communities were determined by Procrustes and Mantel analyses (c). Heatmap showing the connections between the abundances of the ARGs and the bacterial communities at the genus level (30 most common) (d). The urban river and Lake West cocultured with Microcystis aeruginosa, Planktothrix agardhii and control were defined as groups: UM, UP and UC and WM, WP and MC, respectively. The relative abundances of the genera (correlated with the ARGs) among the treatments (n = 4) (e). *, **, and *** indicate significant differences between the bacterial communities and ARG composition at P < 0.05, P < 0.01 and P < 0.001, respectively, by a one-way ANOVA. Data from four replicates (n = 4) are represented as means ± SD.