Metatranscriptomic Evidence for Co-Occurring Top-Down and Bottom-Up Controls on Toxic Cyanobacterial Communities

Abstract

Little is known about the molecular and physiological function of co-occurring microbes within freshwater cyanobacterial harmful algal blooms (cHABs). To address this, community metatranscriptomes collected from the western basin of Lake Erie during August 2012 were examined. Using sequence data, we tested the hypothesis that the activity of the microbial community members is independent of community structure. Predicted metabolic and physiological functional profiles from spatially distinct metatranscriptomes were determined to be >90% similar between sites. Targeted analysis of Microcystis aeruginosa, the historical causative agent of cyanobacterial harmful algal blooms over the past ϳ20 years, as well as analysis of Planktothrix agardhii and Anabaena cylindrica, revealed ongoing transcription of genes involved in microcystin toxin synthesis as well as the acquisition of both nitrogen and phosphorus, nutrients often implicated as independent bottom-up drivers of eutrophication in aquatic systems. Transcription of genes involved in carbon dioxide (CO 2 ) concentration and metabolism also provided support for the alternate hypothesis that high-pH conditions and dense algal biomass result in CO 2 -limiting conditions that further favor cyanobacterial dominance. Additionally, the presence of Microcystis-specific cyanophage sequences provided preliminary evidence of possible top-down virus-mediated control of cHAB populations. Overall, these data provide insight into the complex series of constraints associated with Microcystis blooms that dominate the western basin of Lake Erie during summer months, demonstrating that multiple environmental factors work to shape the microbial community. F reshwater ecosystems are considered among the most endangered in the biosphere (1). One threat to fresh waters around the world is the now nearly annual occurrence of blooms of toxic cyanobacteria. Molecular signatures of cyanobacterial harmful algal blooms (cHABs) have been identified on all seven continents, and these blooms have been occurring with increased frequency and duration in recent years (2-4). The accumulation of bloom biomass has been associated with fish, avian, and mammal intoxication (5, 6); the formation of hypoxic zones (7); the production of taste and odor compounds (8, 9); and even human liver failure in extreme cases (10).The Laurentian Great Lakes are an important freshwater resource, holding ϳ18% of the world's potable water and ϳ84% of the surface waters in North America (11). cHABs have had a persistent presence in Lake Erie and other Laurentian Great Lakes for several decades (3, 12, 13). Nuisance biomass and toxin production associated with cHABs in the Great Lakes have had a detrimental effect not only on ecosystem health but also on the economic health of the surrounding communities; indeed, in August 2014, a bloom event led to the shutdown of the water supply for some ϳ500,000 residents in the region of the city of Toledo, OH (14). To date, research efforts have broadly identified nutrient inputs an...

Biochemistry and genetics of taste- and odor-producing cyanobacteria

“…For example, production of geosmin and 2-MIB by different cyanobacterial strains have been variously linked with light, temperature and nutrient supply (notably phosphorus and nitrogen; Naes et al, 1989;Blevins et al, 1995;Rashash et al, 1995). and Wu et al (1991, for example, hypothesized that cell nitrogen assimilation plays an important role in geosmin production, and indeed recent evidence has demonstrated that nitrogen is coupled with the production of other secondary metabolites such as microcystins and nodularins (Steffen et al, 2015;Davis et al, 2015). Other studies have identified light as a primary driver, reporting relationships between geosmin or 2-MIB production and photosynthetic pigment synthesis Naes et al, 1985;Saadoun et al, 2001;Zhang et al, 2009).…”

Active microbiome structure and its association with environmental factors and viruses at different aquatic sites of a high‐altitude wetland

“…However, other source of diversification in aquatic ecosystems includes biological factors such as viral lysis (Larsen et al., ) or protistan grazing (Jürgens & Matz, ), known as “top‐down control.” So far, little is known about top‐down controllers, such as viruses, which are also expected to affect the active microbial structure in extreme ecosystems such as high‐altitude wetlands. Bottom‐up and top‐down ecosystem forcings were found to act in concert affecting microbial activities of dominant groups, and thus, influence the active community structure in aquatic environments (Pradeep Ram, Chaibi‐Slouma, Keshri, Colombet, & Sime‐Ngando, ; Steffen et al., ). Moreover, bottom‐up and top‐down processes could generate variable effects within different biotic components of the aquatic food‐web under global warming scenarios, changing the net primary production of the system (e.g., Shurin, Clasen, Greig, Kratina, & Thompson, ).…”

Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake

“…The sudden collapse in the D. circinale population strongly implicates an external biological effector, such as viral lysis or bacterial predation, neither of which was addressed at length within the scope this study. In this regard, numerous studies have demonstrated biotic mechanisms for the rapid dispersal of cyanobacteria from surface waters that may explain this observation, including phage-induced lysis (Proctor and Fuhrman, 1990;Williamson et al, 2002;Matteson et al, 2011;Steffen et al, 2015), bacteria-induced lysis (Rashidan and Bird, 2001), grazing by protists (Ger et al, 2014), algicidal compounds (Luo et al, 2013; and cyanobacterial programmed cell death (Franklin, 2014).…”

“…Numerous studies have highlighted the diversity of heterotrophic groups that occur within microbial communities associated with freshwater bloomforming cyanobacteria species (Eiler and Bertilsson, 2004;Wu et al, 2007;Berg et al, 2008;Cheng et al, 2011;Dziallas and Grossart, 2011;Grossart et al, 2011;Wilhelm et al, 2011;Steffen et al, 2012;Woodhouse et al, 2012;Cai et al, 2013;Xing et al, 2013;Bagatini et al, 2014). Further, such studies have demonstrated that, for cyanobacterial-associated microbial communities, despite the identity of these communities being dependent on the cyanobacterial species present (Bagatini et al, 2014), water chemistry, temperature Xing et al, 2013) and ultimately the freshwater system within which the experiment is based, the function of these communities is largely conserved across local and continental spatial scales (Steffen et al, 2012;Penn et al, 2014;Steffen et al, 2015). Fewer studies have assessed how the nature of the cyanobacterial-associated microbial community changes over temporal scales (Wu et al, 2007;Tang et al, 2010;Xing et al, 2013) with changes in cyanobacterial species dominance and biovolume likely to impact on both the composition and function of these groups.…”