Interactions of Toxic Cyanobacteria with Other Aquatic Microbes: Comparison
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Water resources are critically important, but also pose risks of exposure to toxic and pathogenic microbes. Toxic cyanobacteria have been linked to the death and disease of humans, domesticated animals, and wildlife in freshwater systems worldwide. Management approaches successful at reducing cyanobacterial abundance and toxin production have tended to be short-term solutions applied on small scales (e.g., algaecide application) or solutions that entail difficult multifaceted investments (e.g., modification of landscape and land use to reduce nutrient inputs). 

  • cyanotoxin
  • harmful algal bloom (HAB)
  • mycotoxin

1. Introduction

Cyanobacteria are a diverse group of bacteria whose members have been found almost everywhere on Earth, from literally the deepest seas [1] to the driest deserts [2]. Evidence suggests that cyanobacteria were not only among Earth’s earliest lifeforms and the first to be able to photosynthesize but also the ancestors of the chloroplasts within plants [3]. Cyanobacteria comprise much of the base of the food web in aquatic systems, supporting aquatic biodiversity and ecosystem resilience [4]. However, certain cyanobacteria are toxic to humans and other animals [5,6,7,8][5][6][7][8] and proliferate to nuisance abundances in many parts of the world. When this proliferation occurs in a place and time that makes it an immediate threat to human health and the environment, the event is referred to as a Harmful Algal Bloom (HAB).
In inland freshwater lakes, the most common constituents of HABs are toxic cyanobacterial species within the genera Dolichospermum, Aphanizomenon, Microcystis, Planktothrix, and Raphidiopsis [11,12][9][10]. The ability of these species to dominate phytoplankton communities during HABs is often attributed to intrinsic competitive advantages, such as the ability to fix nitrogen and tolerate higher temperatures [13][11], adjust their vertical positions within the water column [14][12], or escape predation [15][13]. Factors such as large rainfall events [16][14] and ballast water exchange [17][15] may, in addition, promote the species’ movement and establishment across landscapes [18,19,20,21,22][16][17][18][19][20]. 

2. Control Methods

The current knowledge of cyanobacterial traits and putative environmental drivers has inspired various methods of controlling HABs that fall roughly within the categories of physical, chemical, and biological. Physical control entails the mechanical inhibition, removal, or elimination of toxic cyanobacteria [23][21]. The use of plankton nets, hand-removal, and coagulants falls within this category [24[22][23],25], as do dam operations in reservoirs (hydrologic control, flushing [20,26][18][24]). Physical control methods also include alteration of the habitat to make it unfavorable for cyanobacterial survival and proliferation. For instance, artificial shading [24[22][25],27], pressurization [28][26], and physical aeration, nanobubble ozonation, or sonication/ultrasound/acoustic cavitation [29,30,31][27][28][29] can be used to physically suppress or damage cyanobacterial cells, and the capping and dredging of aquatic soil and sediment can be used to reduce pre-existing nutrient loads and viable toxic cyanobacterial dormant stages [32,33,34][30][31][32]. Potentially, these methods can be automated or otherwise improved using recent advances in robotic technology and artificial intelligence, such as low-cost unmanned surface vehicles equipped with active suction pumps and mesh-based algae filtration systems [35][33]. Chemical control entails the application of compounds that are harmful to toxic cyanobacteria [36][34]. Artificial compounds such as commercial copper salt solutions [37,38][35][36] are often used, but natural compounds such as methanolic allelochemicals of seaweed are also available [39][37]. The modes of action of these chemical control agents can be direct or indirect. Direct modes include cell lysis and blockage of metabolic processes such as photosynthesis [40][38]. Indirect modes include photosensitivity induction [41][39], removal of growth-limiting nutrients (e.g., with flocculants such as aluminum sulfate to bind growth-limiting nutrients [42][40]), and impedance of colony formation (e.g., with iron reducers such as humic [43][41]). Biological control entails the use of living organisms to keep toxic cyanobacteria in check. These organisms may be brought in from outside the system or manipulated within the system. They may include competitors of toxic cyanobacteria (e.g., green algae and diatoms), which consume cyanobacterial resources and might directly interfere with cyanobacterial survival and reproduction through allelopathy or overgrowth [44,45,46][42][43][44]. The organisms may also include predators, parasites, or pathogens of toxic cyanobacteria, such as planktivorous fish and arthropods [47,48][45][46]. Alternatively, organisms can be installed or manipulated at the edge of the habitat afflicted with toxic cyanobacteria (or in a connected habitat that is upstream) to modify environmental conditions. Examples of this include the planting of cover crops to reduce soil erosion in agricultural systems [49][47], the construction of riparian buffer zones and floating wetlands to curb or counteract influx of nutrients and cyanobacteria from terrestrial sources [49[47][48],50], and the seeding of lake habitats or adjacent riparian buffer zones with organisms capable of diverting, eliminating, or mineralizing nutrients (e.g., submerged aquatic vegetation and filter-feeding bivalves [51,52][49][50]).

3. Interactions of Toxic Cyanobacteria with Other Aquatic Microbes

3.1. Protection and Promotion

Aquatic microbes that consistently benefit toxic cyanobacteria include various species of heterotrophic bacteria and fungi (HBF). Some HBF share intimate and often mutually beneficial symbioses with toxic cyanobacteria. Many of these inhabit the “phycosphere”, the region that immediately surrounds individual cyanobacterial cells [63,64][51][52]. Differing strains of toxic cyanobacteria are known to have distinct HBF assemblages residing in their phycospheres that vary in composition with environmental conditions [65][53]. Microbial interactions in the phycospheres of well-characterized phytoplankton such as Microcystis have been extensively studied in laboratory settings and, to a lesser extent, in the field, and could have significant implications for how to manage cyanobacteria [67,68,69][54][55][56]. In some cases, HBF symbionts are so critical to the ability of toxic cyanobacteria to survive and grow that culturing the cyanobacteria axenically requires special effort [70,71][57][58]. While the precise mechanisms have yet to be resolved, phycospheric heterotrophic bacteria such as in the genus Aeromonas have been found to induce and support colony formation in Microcystis aeruginosa via secretion of signaling compounds and extracellular polymeric substances [70,72,73][57][59][60]. These compounds are crucial in colony formation, which entails the aggregation, functional arrangement, and adherence of cells, along with the construction of surrounding mucilage. The process provides cyanobacteria not only with improved nutrient uptake efficiencies [73][60] but also with resistance to algaecides [74][61] and disinfectants [75][62]. Similarly, heterotrophic bacteria within the genus Rhizobium stimulate the growth of M. aeruginosa by solubilizing phosphorus and decomposing hydrogen peroxide [76,77][63][64], with the latter being both a natural toxic byproduct of aerobic photosynthesis [78][65] and an algaecide used by humans to control HABs [79][66]. Fungi beneficial to toxic cyanobacteria are commonly known to be part of terrestrial symbioses such as toxin-producing lichens [80[67][68],81], but have not often been reported in equivalent symbioses with toxic cyanobacteria in aquatic systems (meaning, in relationships that are protracted, coevolved, and reliant on spatial or temporal proximity). This may be because fungal benefits that enable cyanobacteria to thrive on land (e.g., hyphal substrate degradation and increased desiccation tolerance [82][69]) are less useful to cyanobacteria in water. Nevertheless, there is evidence, both experimentally created [83][70] and observed [84,85][71][72], of fungi within the genus Aspergillus providing cyanobacteria within the genus Nostoc with benefits that include oxidative stress resistance comparable to the previously mentioned (bacteria-conferred) protection against hydrogen peroxide. Moreover, free-living “white-rot” fungi have been shown to drive transformations of common herbicides such as diuron and atrazine, rendering the herbicides subsequently non-lethal to cyanobacteria [86][73].

3.2. Antagonism and Inhibition

Although interactions with other aquatic microbes can be beneficial to toxic cyanobacteria, they can also be detrimental. Pathogens and parasites of grazers can increase, rather than decrease, consumption of toxic cyanobacteria by conferring toxin resistance to their hosts [93][74] or force their hosts to feed more frequently and less discriminately to compensate for the losses of nutrients and energy associated with their infection [94][75]. Decomposers can constrain, rather than promote, HAB formation, either by remineralizing nutrients instead of recycling them so that they are less available to cyanobacteria [95,96,97][76][77][78] or by metabolizing cyanobacterial osmoprotectants (chemicals that enable microbes to cope with osmotic stress [98][79]) and signaling compounds (chemicals that enable microbes to send and receive information about their respective internal and external conditions to and from one another, including for the purpose of quorum sensing [99][80]). The latter, in the cases of dimethylsulfoniopropionate (osmoprotectant) and dimethylsulfide (signaling compound), not only interferes with cyanobacterial use and retention of sulfur but also prevents various micronutrients from traversing cyanobacterial cell membranes [100,101][81][82].

Various microbes have also been found to cause direct harm to toxic cyanobacteria as predators, parasites, or allelopathic competitors, and have subsequently garnered attention as prospective biological control agents against HABs. Theoretically, these species would be better equipped to keep up with the growth, mutation, and dispersal rates of toxic cyanobacteria than most macroscopic control agents, since they, as fellow microbes, are more like the cyanobacteria in each of these respects. Moreover, their size, capacity for asexual reproduction, and relative metabolic flexibility would make them more amenable to being grown in large batches, transported, and dispensed where needed. Candidate microbial biological control agents include cyanophages (host-specific viral pathogens of cyanobacteria such as LPP-1 [102,103,104,105,106][83][84][85][86][87] and microzooplankton (unicellular and metazoan eukaryotes less than 200 µm in size that feed on other organisms, which include protozoan nanoflagellates [107,108][88][89]), as well as several kinds of HBF. The potential efficacy and limitations of each of these groups as biological control agents have been thoroughly summarized elsewhere [20,109[18][90][91][92],110,111], with their major strengths including tailorable specificity (from strain-specific to phylum-specific) and useable sublethal effects (e.g., reduction in mechanical stiffness, inhibited growth, and impaired or dysregulated photosynthesis) and their major weaknesses including lack of scalability from laboratory to field settings given present technology and vulnerability to abiotic extracellular conditions (e.g., pH, temperature, and solar radiation) and biological factors such as bacterial restriction endonucleases and exopolysaccharides, and competing pathogens or virophages (viruses that obligately coinfect hosts with other viruses).

4. Prospects for Incorporating Microbial Species Interactions into the Management of Toxic Cyanobacteria

4.1. Non-Targeted Approaches

Toxic cyanobacteria, pathogenic enteric bacteria, toxic fungi, and parasitic protozoa often display similar distribution patterns and responses to environmental conditions, including correlative associations with factors such as agricultural and wastewater runoff [117,118][93][94]. As such, carefully designed runoff and wastewater management interventions may be sufficient to address all or most of these microbial threats simultaneously [119,120,121][95][96][97]. Where landscape development is feasible, these might include the creation or restructuring of bioswales [122][98] and urban greenspace [123][99] to reduce nutrient pollution and fecal contamination.

4.2. Targeting of Facilitators

Targeting of facilitators to manage toxic cyanobacteria would be a variation on the theme of classical biological control, wherein, instead of introducing or promoting species that are antagonistic to toxic cyanobacteria (at carefully selected times and locations), one would neutralize the species responsible for the cyanobacteria’s vitality and resistance to targeted intervention. It could entail using antimicrobial substances or natural enemies that harm the facilitating associates of toxic cyanobacteria where circumstances prevent the application of algaecides or cyanobacteria-specific control methods. The reported effectiveness of fungicides for controlling cyanobacterial outbreaks on Bermuda grass putting-green surfaces might be viewed as evidence of this principle having already been applied [132][100].

4.3. Reduction of Benthic Occupancy and Recruitment

In terrestrial systems, “seed banks” are the assemblages of plant seeds found in parts of the soil where seeds can safely remain dormant until there are signs of favorable growth conditions above-ground. Seed banks can enable terrestrial weeds to continuously re-infest habitats, even in the face of dedicated above-ground control efforts [137,138][101][102]. Methods involving manipulation of seed banks to control weeds include using (soil-applied) chemicals to stimulate premature germination, solarization (placement of a transparent tarp across a soil bed to desiccate weeds and seeds through the green-house effect), and introduction or stimulation of microorganisms that rapidly colonize and kill/impair seeds prior to germination via chemotaxis (direct movement in response to a gradient of increasing or decreasing concentration of a chemical cue, in this case the “scent” of the target seeds [137][101]). In aquatic systems, benthic sediments can house seed banks as well, comprising not only the seeds of submerged aquatic vegetation and other aquatic plants but also the dormant stages of phytoplankton, heterotrophic bacteria, and fungi (akinetes, heterocysts, and spores [139,140][103][104]. Overwintering and benthic recruitment from these aquatic seed banks are thought to be important origins of source populations for HABs and other large summer populations of cyanobacteria [141][105] and, in some cases, appear to be linked to toxicity [142,143][106][107].

4.4. Manipulation of Natural Enemies

Natural enemies (predators, parasites, or pathogens) of weeds and pests are intuitive choices for use as biological control agents against these organisms but must be screened and employed carefully. Ideally, they are native to the habitat and specialized to feed on the target (prey-/host-specific), to avoid the possibility of they themselves becoming invasive or being ineffective in controlling their targets. The same principles apply in the case of biological control of toxic cyanobacteria. For example, free-living freshwater amoeba such as Acanthamoeba castellanii feed and grow efficiently on toxic cyanobacteria but are also parasites of humans and potential reservoirs of opportunistic pathogens [148][108]. To reduce the likelihood of toxic cyanobacteria adapting to individual control agents, two or more can be employed simultaneously or in sequence to create conflicting requirements for adaptation (opposing selection pressures). For example, planktivorous grazers deterred by cyanobacterial toxins, colony formation, or filamentous growth forms can be introduced in conjunction with HBF that disrupt these defense mechanisms. Some of these HBF may be beneficial symbionts of the grazers (gut microfauna or transient “probiotics” [153,154,155][109][110][111]). Others may be free-living HBF that reduce the “harmfulness” of HAB-forming cyanobacteria by degrading cyanobacterial toxins (e.g., microcystin-LR, cylindrospermopsin, and saxitoxin [156,157,158][112][113][114]). This would be akin to how indigenous soil bacteria such as Pseudomonas putida J1 are employed (via the aeration of the soil) to neutralize allelopathic compounds of terrestrial plants, such as the juglone exuded from the roots of black walnut trees [159][115]

5. Conclusions

Harmful algal blooms (HABs) of toxic cyanobacteria are a complex environmental issue, with far-reaching ecological, socioeconomic, and human health consequences that may be increasing in severity as time goes on. The fact that previous methodologies to resolve it have yielded mixed results suggests that there may be case-specific nuances to account for in every HAB-afflicted aquatic system and that novel approaches must be developed that incorporate them. However, it should not be forgotten that HABs of the same kind occur globally and are already a serious problem [191,192][116][117]. Even amidst the case-specific nuances and differences [193,194[118][119][120],195], there must be shared conditions and processes for the global patterns in HAB occurrence to be observed, perhaps most conspicuously within the dynamics of the ecological species interactions within these systems. As such, it remains appropriate to leverage what is known, refine and utilize all available tools, and develop appropriately multifaceted approaches to managing HABs across various systems. This includes consideration of the reality that, although faster, more aggressive control methods may thoroughly eliminate target species such as toxic cyanobacteria, methods that allow the species to remain within the system and exhibit small-amplitude population cycles can be more cost-effective and more conducive to ensuring ecosystem resilience [196,197,198][121][122][123].

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