Algal blooms as biofilm analogues: Evolutionary insights into cyanobacterial adaptation

Cyanobacteria have evolved a wide range of ecological strategies spanning billions of years, including benthic mat formation, symbiotic lifestyles, and planktonic dominance in diverse aquatic systems. We reexamined the ecological and evolutionary drivers of bloom formation, with particular emphasis on the roles of cyanobacterial-bacterial and viral interactions, microbial community dynamics, and genetic diversification in shaping bloom ecology. We propose that algal blooms function as ecological analogues of biofilms for bloom-forming cyanobacteria, providing a structured, metabolically active microenvironment that counters environmental stress via production of extracellular polymeric substances and carotenoids, and formation of an interactive microbial consortial phycosphere. This facilitates cell to cell communication and horizontal gene transfer, and accelerates adaptive genetic diversification. Framing cyanobacterial blooms within this evolutionary and functional context offers new perspectives on their proliferation and persistence, resilience, and ecological significance; with implications for understanding bloom dynamics and developing more effective harmful algal bloom mitigation strategies. Cyanobacteria are the oldest oxygenic phototrophs on Earth, with fossil records extending back to Archean Eon (Golubic and Seong-Joo 1999; Schirrmeister et al. 2015). Many lineages form mats that thrive in benthic and epilithic habitats, where attachment and stability confer clear ecological advantages (Chen et al. 2021; Paerl et al. 2000). Over evolutionary time, some cyanobacterial groups transitioned to a planktonic lifestyle, dispersing throughout the photic water column, providing habitat expansion (Chen et al. 2021). Primary production of current marine and freshwater pelagic habitats is dominated by free-living picocyanobacteria, which are highly adapted to this vast and often oligotrophic environment (Flombaum et al. 2013). Among the free-living cyanobacteria, certain species evolved with the remarkable ability to aggregate and form dense surface blooms. Based on a comparative genome analysis, these lineages were likely established around 1 ± 0.5 billion years ago (Schirrmeister et al. 2015). Because the formation of massive surface blooms is recognized as a threat to ecosystem and biotic health and hence a management challenge, the mechanisms underlying bloom development, proliferation, and collapse have been extensively investigated, largely in freshwater ecosystems (Huisman et al. 2018). The transition to a surface-associated lifestyle among bloom-forming cyanobacteria involves substantial physiological and metabolic reprogramming (Huang et al. 2025). In Microcystis, a widely-distributed and studied bloom-forming cyanobacterium, colony buoyancy and aggregation are regulated predominantly through the coordinated functions of gas vesicles and extracellular polymeric substances (EPS) (Wei et al. 2019). During early stages of bloom formation, cells proliferate rapidly within the water column, and surface accumulation generally occurs only after the population exceeds a critical density, suggesting the involvement of quorum sensing or other cell-to-cell communication mechanisms (Li et al. 2013; Ramsay and Salmond 2012). These observations suggest that intercellular communication and EPS production are central processes in Microcystis bloom formation, paralleling key features of bacterial biofilm development (Shen et al. 2011). Accordingly, we propose that cyanobacterial surface blooms function as ecological analogues of biofilms: an adaptive strategy that enhances community resilience, facilitates gene and metabolite exchange, and accelerates genetic diversification in response to environmental challenges (Fig. 1). Biofilms enhance cellular protection and survival by embedding cells within EPS that acts as a physical and chemical barrier against environmental stressors such as antibiotics, toxins, UV radiation, and predation (Flemming and Wingender 2010). This matrix limits the penetration of harmful agents, stabilizes local microenvironments, and promotes cooperative interactions, collectively increasing microbial community resilience and persistence, while likely remaining selective for certain gases and essential simple molecules such as key macro and micro nutrients, amino acids, vitamins, and metals (Fig. 1). In bloom-forming cyanobacteria, occupation of the water surface as colonies confers several ecological advantages, including enhanced access to light and atmospheric carbon dioxide, recycled nutrient supply, protection from chemical stressors and grazing, and the ability to suppress competitors (Paerl and Millie 1996; Xiao et al. 2018). These benefits, however, are counterbalanced by increased exposure to ultraviolet radiation and reactive oxygen species (ROS), which exert oxidative stress and require the deployment of effective photoprotective and antioxidant defense mechanisms (i.e., carotenoids) (Paerl et al. 1985). This physiological trade-off highlights a finely tuned balance between rapid growth within the water column and survival at the surface, enabling bloom-forming cyanobacteria to persist and dominate even under unfavorable environmental conditions. Accordingly, bloom formation represents an ecological trait shaped by natural selection, and the capacity to form blooms has been positively selected during the evolution of bloom-forming cyanobacterial species (Fig. 1). Biofilms create microenvironmental gradients due to limited diffusion within the dense extracellular matrix, which combined with localized metabolic activity, leads to uneven consumption and production of oxygen, nutrients, and metabolites (Flemming and Wingender 2010). As a result, steep gradients in oxygen, pH, redox conditions, and substrate availability develop over micrometer scales within the biofilm (Paerl et al. 2000). Cyanobacterial surface blooms create microenvironmental gradients through dense cell aggregation and light-intensity-dependent photosynthetic activity. By forming a surface-active material at the water surface, Microcystis colonies can counteract wind-driven mixing and reduce subsurface water velocity, thereby stabilizing the local environment and limiting physical disruption of the bloom (Wu et al. 2019). Limited mixing within surface scums may further enhance these gradients, producing sharp vertical heterogeneity in physicochemical conditions within the bloom. Intense surface blooms often lead to high pH levels due to drawdown of carbon dioxide, leading to potential carbon limitation. However, a surface existence optimizes exposure to atmospheric carbon dioxide, which is steadily increasing due to anthropogenic enrichment, potentially alleviating carbon limitation (Paerl and Ustach 1982). However, in contrast to cyanobacterial mats, very little is known about microenvironmental gradients in the surface scum of blooms (Paerl et al. 2000). Fang et al. (2014) showed that increasing irradiance elevates dissolved oxygen and pH while reducing oxidation–reduction potential. Under conditions of high irradiance and elevated temperature, photosynthetic activity in cyanobacterial biomass declines, suggesting that bloom-forming cells are subjected to photoinhibition and/or oxidative stress associated with excessive light exposure. At low irradiance, oxygen diffuses from the surrounding water into the biomass, whereas at high irradiance, enhanced photosynthesis reverses the gradient, causing oxygen to diffuse into the surrounding water. Strong sunlight can enhance the production of ROS in the bloom biomass (Paerl and Otten 2013). Urakawa et al. (2021) reported that cyanobacterial blooms can generate high concentrations of hydrogen peroxide within a thin surface water layer (5–60 mm). Cyanobacterial surface scums can also absorb substantial solar radiation, leading to elevated temperatures within the bloom zone (Urakawa et al. 2021). Localized warming is ecologically significant because cyanobacteria generally exhibit high optimal growth temperatures. Consequently, heat retention within surface blooms can further enhance cyanobacterial competitive dominance by selectively favoring their growth and metabolic activity while suppressing less thermotolerant eukaryotic phytoplankton taxa (Paerl and Huisman 2009). Biofilms exhibit community cooperation and functional specialization through the formation of physiologically distinct subpopulations that perform specialized functions, including nutrient acquisition, EPS production, stress tolerance, and detoxification (Flemming and Wingender 2010). These coordinated activities optimize resource use and enhance biofilm stability and survival (Fig. 1). Similarly, bloom-forming cyanobacteria maintain a biofilm analogue microbial community network known as the phycosphere, a nutrient and metabolite rich microenvironment surrounding cyanobacterial cells or colonies; favoring close physical and metabolic interactions between free-living cyanobacteria and a diverse assemblage of heterotrophic bacteria (Hoke et al. 2021; Paerl and Millie 1996), and mediating key biological interactions that regulate bloom initiation, persistence, and toxicity (Paerl and Millie 1996). Phycospheric exchanges of nutrients, metabolites, signaling molecules, and ROS occur between cyanobacteria and their bacterial consorts, influencing growth, colony formation, buoyancy regulation, stress tolerance, and cyanotoxin production (Große et al. 2025; Hoke et al. 2021; Paerl and Millie 1996). Cyanotoxin production may also play functional roles within this densely interactive microenvironment. In the phycosphere context, cyanotoxins may therefore act not only as environmental hazards when released into surrounding waters but also as bioactive metabolites that influence microbial interactions and community structure within the bloom. Clarifying phycosphere processes provides mechanistic insight into bloom dynamics that cannot be resolved at bulk water scales and is essential for developing effective strategies to predict, manage, and mitigate harmful cyanobacterial blooms. Biofilms enhance horizontal gene transfer by maintaining high cell density and close cell-to-cell contact within a stable extracellular matrix, which facilitates conjugation, transformation, and phage-mediated transduction (Flemming and Wingender 2010). The matrix also retains extracellular DNA and mobile genetic elements, increasing the efficiency of genetic exchange within the community (Fig. 1). Accumulated evidence from past studies supports the conclusion that horizontal gene transfer plays a significant role in cyanobacterial surface blooms, which function as biofilm analogues. Phage associated genes are often found in the surface bloom (Krausfeldt et al. 2024; Pound and Wilhelm 2020). For example, M. aeruginosa genomes are highly enriched with insertion sequences (Frangeul et al. 2008; Makarova et al. 2011), which account for as much as 11% of the gene content (Lin et al. 2011), and these elements could bring plasticity into the genomes of M. aeruginosa. Further, a previous study showed that the M. aeruginosa genome contains the largest number of defense genes (n = 492) among 1055 bacterial and archaeal genomes, including the CRISPR (clustered regularly interspaced short palindromic repeats)-Cas systems, classical restriction-modification system, and toxin-antitoxin system (Makarova et al. 2011). Microcystis populations are partially controlled by phage density, and phase-lagged oscillatory dynamics between M. aeruginosa abundance and its cyanophages have been documented (Yoshida et al. 2008). Although viral infections typically become more severe at high host cell densities and under strong irradiance stress, interactions between cyanophages and bloom-forming cyanobacterial cells appear to be more complex than previously recognized. A recent study demonstrated distinct metabolic states and phage–host interaction modes between single-cell and colonial Microcystis, in which lytic infections prevail in single cells and lysogeny predominates in colonial populations (Huang et al. 2025). This observation is noteworthy because cyanophages can facilitate gene shuffling in Microcystis through predominantly lysogenic activity, thereby allowing host cells to survive while maintaining genomic flexibility. Host-like genes are commonly found in viral genomes. Cyanophage Ma-LMM01 carries a host-derived nblA gene coding non-bleaching protein A, which is involved in the degradation of phycobilisomes, the main light-harvesting complexes in cyanobacteria (Yoshida-Takashima et al. 2012). During infection, this cyanophage strongly expresses nblA, promoting phycobilisome degradation. This process can reduce light absorption and help bloom-forming host cells alleviate UV and light-induced stress, thereby benefiting phages and hosts during infection. Based on these observations, interactions between M. aeruginosa and its phages and mobile genetic elements likely extend beyond a simple evolutionary arms race and instead represent a more complex, potentially mutualistic relationship that drives repeated cycles of gene gain and loss within host genomes. Cyanophages appear to have coevolved with M. aeruginosa to facilitate gene shuffling, thereby generating remarkable host genomic diversity that enhances adaptation to and survival under changing environmental conditions. Consequently, surface scum formation is likely an essential life stage of Microcystis following the loss of a biofilm-associated benthic lifestyle, contributing to the maintenance of high genomic flexibility. This raises a broader question: Can the concept of algal blooms as biofilm analogues also be applied to eukaryotic phytoplankton such as dinoflagellates and coccolithophores? These groups also form massive blooms that are often associated with high viral activity (Short 2012). However, unlike many bloom-forming cyanobacteria that primarily proliferate through clonal expansion, eukaryotic phytoplankton frequently possess more complex life cycles that may include sexual reproduction. For example, dinoflagellates such as Karenia brevis may undergo sexual stages during dense bloom conditions, potentially facilitating genetic recombination when large numbers of compatible cells aggregate (Persson et al. 2013). Recent transcriptomic evidence has detected elevated expression of meiosis-related genes during natural dinoflagellate blooms, suggesting that sexual processes may occur during bloom development and contribute to population persistence and diversification (Lin et al. 2022). In such systems, bloom formation may therefore represent not only rapid population growth but also, and perhaps more importantly, ecological opportunities for mating and genetic diversification. Thus, although these organisms belong to a different domain, bloom formation may similarly facilitate close cell-to-cell interactions that promote communication and accelerate adaptive genetic diversification. Cyanobacterial surface bloom formation can be regarded as an evolutionary analogue to biofilm development, a collective, protective, and genetically dynamic state. In biofilms, dense cellular organization promotes horizontal gene transfer, enabling rapid adaptation and metabolic diversification. Similarly, cyanobacterial blooms function as genetic “mutualistic hotspots,” where elevated oxidative stress, steep microenvironmental gradients, and resulting heterogeneity in host physiology, together with high host cell density and abundant lysogenic cyanophages, facilitate frequent recombination and gene flow, thereby accelerating cyanobacterial evolution and community-level adaptation. Consequently, bloom episodes may serve as transient evolutionary laboratories that enhance genetic diversification and resilience in bloom-forming cyanobacteria. Rather than solely being symptoms of eutrophication, cyanobacterial blooms may represent a deeply rooted microbial strategy for survival and dominance. Framing cyanobacterial blooms as biofilm analogues within an evolutionary and functional context provides new perspectives on their persistence, resilience, and ecological significance. This perspective has important implications for improving prediction and mechanistic models of bloom dynamics, as well as for developing more effective bloom mitigation strategies. Hidetoshi Urakawa and Hans W. Paerl developed the concept. Hidetoshi Urakawa conducted the literature review and drafted the manuscript, and Hans W. Paerl contributed to manuscript writing, revision and reference selection. This research was partially supported to Hidetoshi Urakawa by a grant (W81EWF-22-HAB-BAA) from the U.S. Army Engineer Research and Development Center (ERDC) under a Cooperative Agreement (W912HZ-24-2-0002), administered through the South Florida Water Management District (SFWMD Agreement No. 4600004941), and through additional support from the Harmful Algal Bloom Demonstration Program (W912HZ24SC001, contract CSO-HAB-2024-0005), also funded by the U.S. Army ERDC. Hans W. Paerl was supported by the U.S. National Science Foundation (projects 1840715, 2108917, 2418066) and the U.S. National Institutes of Health (2P01ES028939-06). None declared. No new data were generated or analyzed in this study.