Duelling 'CyanoHABs': Unravelling the environmental drivers controlling dominance and succession among diazotrophic and non-N2-fixing harmful cyanobacteria

Eutrophication often manifests itself by increased frequencies and magnitudes of cyanobacterial harmful algal blooms (CyanoHABs) in freshwater systems. It is generally assumed that nitrogen-fixing cyanobacteria will dominate when nitrogen (N) is limiting and non-N2 fixers dominate when N is present in excess. However, this is rarely observed in temperate lakes, where N2 fixers often bloom when N is replete, and non-fixers (e.g. Microcystis) dominate when N concentrations are lowest. This review integrates observations from previous studies with insights into the environmental factors that select for CyanoHAB groups. This information may be used to predict how nutrient reduction strategies targeting N, phosphorus (P) or both N and P may alter cyanobacterial community composition. One underexplored concern is that as N inputs are reduced, CyanoHABs may switch from non-N2 fixing to diazotrophic taxa, with no net improvement in water quality. However, monitoring and experimental observations indicate that in eutrophic systems, minimizing both N and P loading will lead to the most significant reductions in total phytoplankton biomass without this shift occurring, because successional patterns appear to be strongly driven by physical factors, including temperature, irradiance and hydrology. Notably, water temperature is a primary driver of cyanobacterial community succession, with warming favouring non-diazotrophic taxa

Mitigating the Expansion of Harmful Algal Blooms Across the Freshwater-to-Marine Continuum

Anthropogenic nutrient overenrichment, coupled with rising temperatures, and an increasing frequency of extreme hydrologic events (storms and droughts) are accelerating eutrophication and promoting the expansion of harmful algal blooms (HABs) across the freshwater-to-marine continuum. All HABs - with a focus here on cyanobacterial blooms - pose serious consequences for water supplies, fisheries, recreational uses, tourism, and property values. As nutrient loads grow in watersheds, they begin to compound the effects of legacy stores. This has led to a paradigm shift in our understanding of how nutrients control eutrophication and blooms. Phosphorus (P) reductions have been traditionally prescribed exclusively for freshwater systems, while nitrogen (N) reductions were mainly stressed for brackish and coastal waters. However, because most systems are hydrologically interconnected, single nutrient (e.g., P only) reductions upstream may not necessarily reduce HAB impacts downstream. Reducing both N and P inputs is the only viable nutrient management solution for long-term control of HABs along the continuum. This article highlights where paired physical, chemical, or biological controls may improve beneficial uses in the short term, and offers management strategies that should be enacted across watershed scales to combat the global expansion of HABs across geographically broad freshwater-to-marine continua

The molecular ecology of Microcystis sp. blooms in the San Francisco Estuary

Harmful blooms of the cyanobacterium Microcystis sp. have become increasingly pervasive in the San Francisco Estuary Delta (USA) since the early 2000s and their rise has coincided with substantial decreases in several important fish species. Direct and indirect effects Microcystis blooms may have on the Delta food web were investigated. The Microcystis population was tracked for 2 years at six sites throughout the Delta using quantitative PCR. High-throughput amplicon sequencing and colony PCR sequencing revealed the presence of 10 different strains of Microcystis, including 6 different microcystin-producing strains. Shotgun metagenomic analysis identified a variety of Microcystis secondary metabolite pathways, including those for the biosynthesis of: aeruginosin, cyanopeptolin, microginin, microviridin and piricyclamide. A sizable reduction was observed in microbial community diversity during a large Microcystis bloom (H′ = 0.61) relative to periods preceding (H′ = 2.32) or following (H′ = 3.71) the bloom. Physicochemical conditions of the water column were stable throughout the bloom period. The elevated abundance of a cyanomyophage with high similarity to previously sequenced isolates known to infect Microcystis sp. was implicated in the bloom's collapse. Network analysis was employed to elucidate synergistic and antagonistic relationships between Microcystis and other bacteria and indicated that only very few taxa were positively correlated with Microcystis

A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp.

This review summarizes the present state of knowledge regarding the toxic, bloom-forming cyanobacterium, Microcystis, with a specific focus on its geographic distribution, toxins, genomics, phylogeny, and ecology. A global analysis found documentation suggesting geographic expansion of Microcystis, with recorded blooms in at least 108 countries, 79 of which have also reported the hepatatoxin microcystin. The production of microcystins (originally “Fast-Death Factor”) by Microcystis and factors that control synthesis of this toxin are reviewed, as well as the putative ecophysiological roles of this metabolite. Molecular biological analyses have provided significant insight into the ecology and physiology of Microcystis, as well as revealed the highly dynamic, and potentially unstable, nature of its genome. A genetic sequence analysis of 27 Microcystis species, including 15 complete/draft genomes are presented. Using the strictest biological definition of what constitutes a bacterial species, these analyses indicate that all Microcystis species warrant placement into the same species complex since the average nucleotide identity values were above 95%, 16S rRNA nucleotide identity scores exceeded 99%, and DNA–DNA hybridization was consistently greater than 70%. The review further provides evidence from around the globe for the key role that both nitrogen and phosphorus play in controlling Microcystis bloom dynamics, and the effect of elevated temperature on bloom intensification. Finally, highlighted is the ability of Microcystis assemblages to minimize their mortality losses by resisting grazing by zooplankton and bivalves, as well as viral lysis, and discuss factors facilitating assemblage resilience

Mitigating a global expansion of toxic cyanobacterial blooms: Confounding effects and challenges posed by climate change

Managing and mitigating the global expansion of toxic cyanobacterial harmful algal blooms (CyanoHABs) is a major challenge facing researchers and water resource managers. Various approaches, including nutrient load reduction, artificial mixing and flushing, omnivorous fish removal, algaecide applications and sediment dredging, have been used to reduce bloom occurrences. However, managers now face the additional challenge of having to address the effects of climate change on watershed hydrological and nutrient load dynamics, water temperature, mixing regime and internal nutrient cycling. Rising temperatures and increasing frequencies and magnitudes of extreme weather events, including tropical cyclones, extratropical storms, floods and droughts, all promote CyanoHABs and affect the efficacy of ecosystem remediation measures. These climatic changes will likely require setting stricter nutrient (including both nitrogen and phosphorus) reduction targets for bloom control in affected waters. In addition, the efficacy of currently used methods to reduce CyanoHABs will need to be re-evaluated in light of the synergistic effects of climate change with nutrient enrichment

Mitigating eutrophication and toxic cyanobacterial blooms in large lakes: The evolution of a dual nutrient (N and P) reduction paradigm

Cyanobacterial harmful algal blooms (CyanoHABs) are an increasingly common feature of large, eutrophic lakes. Non-N2-fixing CyanoHABs (e.g., Microcystis) appear to be proliferating relative to N2-fixing CyanoHABs in systems receiving increasing nutrient loads. This shift reflects increasing external nitrogen (N) inputs, and a > 50-year legacy of excessive phosphorus (P) and N loading. Phosphorus is effectively retained in legacy-impacted systems, while N may be retained or lost to the atmosphere in gaseous forms (e.g., N2, NH3, N2O). Biological control on N inputs versus outputs, or the balance between N2 fixation versus denitrification, favors the latter, especially in lakes undergoing accelerating eutrophication, although denitrification removal efficiency is inhibited by increasing external N loads. Phytoplankton in eutrophic lakes have become more responsive to N inputs relative to P, despite sustained increases in N loading. From a nutrient management perspective, this suggests a need to change the freshwater nutrient limitation and input reduction paradigms; a shift from an exclusive focus on P limitation to a dual N and P co-limitation and management strategy. The recent proliferation of toxic non-N2-fixing CyanoHABs, and ever-increasing N and P legacy stores, argues for such a strategy if we are to mitigate eutrophication and CyanoHAB expansion globally

Global solutions to regional problems: Collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study

In early August 2014, the municipality of Toledo, OH (USA) issued a ‘do not drink’ advisory on their water supply directly affecting over 400,000 residential customers and hundreds of businesses (Wilson, 2014). This order was attributable to levels of microcystin, a potent liver toxin, which rose to 2.5 μg L−1 in finished drinking water. The Toledo crisis afforded an opportunity to bring together scientists from around the world to share ideas regarding factors that contribute to bloom formation and toxigenicity, bloom and toxin detection as well as prevention and remediation of bloom events. These discussions took place at an NSF- and NOAA-sponsored workshop at Bowling Green State University on April 13 and 14, 2015. In all, more than 100 attendees from six countries and 15 US states gathered together to share their perspectives. The purpose of this review is to present the consensus summary of these issues that emerged from discussions at the Workshop. As additional reports in this special issue provide detailed reviews on many major CHAB species, this paper focuses on the general themes common to all blooms, such as bloom detection, modeling, nutrient loading, and strategies to reduce nutrients