Microbiota under bloom stress: A review and meta-analysis of bloom-associated cyanopeptides, environmental stressors, and microbial shifts in free-living and host gut microbiomes.

Abstract

Cyanobacterial blooms are intensifying globally due to nutrient enrichment and climate change, producing a chemically diverse suite of peptides, in addition to the well-studied microcystins. These cyanopeptides, including anabaenopeptins, cyanopeptolins, aeruginosins, and microginins, frequently co-occur in blooms across freshwater and estuarine systems and exhibit potent protease- and phosphatase-inhibitory activities at environmentally relevant concentrations. This review synthesizes emerging evidence that these compounds may profoundly influence both environmental and host-associated microbiota. Bloom-associated cyanopeptides and related environmental stressors may act as ecological filters in aquatic ecosystems, contributing to microbial dysbiosis, which is characterized by changes in community composition and sometimes reduced diversity. This also leads to the enrichment of toxin-degrading components of microbiota taxa, such as Sphingomonas and Novosphingobium, and metabolic reconfiguration toward xenobiotic degradation. Microbiota exposed to bloom-associated cyanopeptides rich conditions in aquatic ecosystems occur in free and particulate forms in the water column, and these forms often recover and adapt more rapidly than host-associated microbiomes. However, conflicting results have been observed in fish gut microbiota data responses, where some host-associated microbiomes show relatively fast recovery and others show delayed restoration. Multi-omics studies have revealed conserved mechanisms linking cyanopeptide exposure to shifts in microbial structure and metabolic pathways, which together can affect host physiology. However, most studies remain biased toward microcystin-LR, and there is a significant gap in our understanding of how other cyanopeptides alter free-living and host gut microbiota in aquatic ecosystems. Therefore, this review identifies an important next step in research, which should focus on how non-microcystin cyanopeptides affect free and host-gut microbiota, and these studies should include multiomics approaches to unravel these changes under natural field observations and controlled exposure. Recognizing microbiota as both targets and agents of cyanopeptide transformation offers a new framework for understanding bloom ecology, because this knowledge will aid in predicting ecosystem recovery and mitigating the ecological risks of these compounds.