Abstract
Interactions between microorganisms and algae during bloom events significantly impacts their physiology, alters ambient chemistry, and shapes ecosystem diversity. The potential role these interactions have in bloom development and decline are also of particular interest given the ecosystem impacts of algal blooms. We hypothesized that microbial community structure and succession is linked to specific bloom stages, and reflects complex interactions among taxa comprising the phycosphere environment. This investigation used pyrosequencing and correlation approaches to assess patterns and associations among bacteria, archaea, and microeukaryotes during a spring bloom of the dinoflagellate Alexandrium catenella. Within the bacterial community, Gammaproteobacteria and Bacteroidetes were predominant during the initial bloom stage, while Alphaproteobacteria, Cyanobacteria, and Actinobacteria were the most abundant taxa present during bloom onset and termination. In the archaea biosphere, methanogenic members were present during the early bloom period while the majority of species identified in the late bloom stage were ammonia-oxidizing archaea and Halobacteriales. Dinoflagellates were the major eukaryotic group present during most stages of the bloom, whereas a mixed assemblage comprising diatoms, green-algae, rotifera, and other microzooplankton were present during bloom termination. Temperature and salinity were key environmental factors associated with changes in bacterial and archaeal community structure, respectively, whereas inorganic nitrogen and inorganic phosphate were associated with eukaryotic variation. The relative contribution of environmental parameters measured during the bloom to variability among samples was 35.3%. Interaction analysis showed that Maxillopoda, Spirotrichea, Dinoflagellata, and Halobacteria were keystone taxa within the positive-correlation network, while Halobacteria, Dictyochophyceae, Mamiellophyceae, and Gammaproteobacteria were the main contributors to the negative-correlation network. The positive and negative relationships were the primary drivers of mutualist and competitive interactions that impacted algal bloom fate, respectively. Functional predictions showed that blooms enhance microbial carbohydrate and energy metabolism, and alter the sulfur cycle. Our results suggest that microbial community structure is strongly linked to bloom progression, although specific drivers of community interactions and responses are not well understood. The importance of considering biotic interactions (e.g., competition, symbiosis, and predation) when investigating the link between microbial ecological behavior and an algal bloom’s trajectory is also highlighted.
Highlights
Phytoplankton are a fundamental component of the marine ecosystem, playing multiple roles in matter cycling and the support of global biological and geochemical processes (Lindh et al, 2013)
Our analysis focused on documenting microbial community structure during algal blooms, and identifying specific associations among bacteria, archaea, and microeukaryotes to provide insights into mechanisms underlying microbial interactions and dynamics
These results indicate that temperature was the major abiotic force shaping microbial community structure in Salt Pond, which is consistent with past studies that documented a pronounced impact of temperature on plankton composition (Niu et al, 2011; Hampton et al, 2014; Frenken et al, 2016)
Summary
Phytoplankton are a fundamental component of the marine ecosystem, playing multiple roles in matter cycling and the support of global biological and geochemical processes (Lindh et al, 2013). Phytoplankton can be a double-edged sword, ecologically speaking. Phytoplankton account for less than 1% of overall photosynthetic biomass on Earth, yet contribute at least half of the world’s net oxygen production (Field et al, 1998; Monier et al, 2015). Some phytoplankton taxa form harmful algal blooms (HABs), which can adversely impact ecosystems and human health. Alexandrium is a cosmopolitan dinoflagellate genus that proliferates annually worldwide, often forming dense blooms in near-shore waters. Blooms of certain toxin-producing species in these genus are responsible for widespread and significant impacts, including animal mortality events, and can contaminate shellfish with toxins that threaten human health (Bagatini et al, 2014). Estimates of the economic costs of these blooms exceed $20 million USD (Anderson et al, 2012), largely due to losses suffered by tourism and aquaculture industries
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