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Molecular insights into a dinoflagellate bloom.

ABSTRACT: In coastal waters worldwide, an increase in frequency and intensity of algal blooms has been attributed to eutrophication, with further increases predicted because of climate change. Yet, the cellular-level changes that occur in blooming algae remain largely unknown. Comparative metatranscriptomics was used to investigate the underlying molecular mechanisms associated with a dinoflagellate bloom in a eutrophied estuary. Here we show that under bloom conditions, there is increased expression of metabolic pathways indicative of rapidly growing cells, including energy production, carbon metabolism, transporters and synthesis of cellular membrane components. In addition, there is a prominence of highly expressed genes involved in the synthesis of membrane-associated molecules, including those for the production of glycosaminoglycans (GAGs), which may serve roles in nutrient acquisition and/or cell surface adhesion. Biotin and thiamine synthesis genes also increased expression along with several cobalamin biosynthesis-associated genes, suggesting processing of B12 intermediates by dinoflagellates. The patterns in gene expression observed are consistent with bloom-forming dinoflagellates eliciting a cellular response to elevated nutrient demands and to promote interactions with their surrounding bacterial consortia, possibly in an effort to cultivate for enhancement of vitamin and nutrient exchanges and/or direct consumption. Our findings provide potential molecular targets for bloom characterization and management efforts.

SUBMITTER: Gong W

PROVIDER: S-EPMC5270570 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Molecular insights into a dinoflagellate bloom.

Gong Weida W Browne Jamie J Hall Nathan N Schruth David D Paerl Hans H Marchetti Adrian A

The ISME journal 20161209 2

In coastal waters worldwide, an increase in frequency and intensity of algal blooms has been attributed to eutrophication, with further increases predicted because of climate change. Yet, the cellular-level changes that occur in blooming algae remain largely unknown. Comparative metatranscriptomics was used to investigate the underlying molecular mechanisms associated with a dinoflagellate bloom in a eutrophied estuary. Here we show that under bloom conditions, there is increased expression of m ...[more]

PMID: 27935592

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Project description: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.

Project description:The development and demise of a harmful algal bloom (HAB) are generally regulated by multiple processes; identifying specific critical drivers for a specific bloom is important yet challenging. Here, we conducted a whole-assemblage molecular ecological study on a dinoflagellate bloom to address the hypothesis that energy and nutrient acquisition, defense against grazing and microbial attacks, and sexual reproduction are critical to the rise and demise of the bloom. Microscopic and molecular analyses identified the bloom-causing species as Karenia longicanalis and showed that the ciliate Strombidinopsis sp. was dominant in a nonbloom plankton community, whereas the diatom Chaetoceros sp. dominated the after-bloom community, along with remarkable shifts in the community structure for both eukaryotes and prokaryotes. Metatranscriptomic analysis indicated that heightened energy and nutrient acquisition in K. longicanalis significantly contributed to bloom development. In contrast, active grazing by the ciliate Strombidinopsis sp. and attacks by algicidal bacteria (Rhodobacteracea, Cryomorphaceae, and Rhodobacteracea) and viruses prevented (at nonbloom stage) or collapsed the bloom (in after-bloom stage). Additionally, nutrition competition by the Chaetoceros diatoms plausibly contributed to bloom demise. The findings suggest the importance of energy and nutrients in promoting this K. longicanalis bloom and the failure of antimicrobial defense and competition of diatoms as the major bloom suppressor and terminator. This study provides novel insights into bloom-regulating mechanisms and the first transcriptomic data set of K. longicanalis, which will be a valuable resource and essential foundation for further elucidation of bloom regulators of this and related species of Kareniaceae in the future. IMPORTANCE HABs have increasingly occurred and impacted human health, aquatic ecosystems, and coastal economies. Despite great efforts, the factors that drive the development and termination of a bloom are poorly understood, largely due to inadequate in situ data about the physiology and metabolism of the causal species and the community. Using an integrative molecular ecological approach, we determined that heightened energy and nutrient acquisition promoted the bloom, while resource allocation in defense and failure to defend against grazing and microbial attacks likely prevented or terminated the bloom. Our findings reveal the differential roles of multiple abiotic and biotic environmental factors in driving the formation or demise of a toxic dinoflagellate bloom, suggesting the importance of a balanced biodiverse ecosystem in preventing a dinoflagellate bloom. The study also demonstrates the power of whole-assemblage metatranscriptomics coupled to DNA barcoding in illuminating plankton ecological processes and the underlying species and functional diversities.

Project description:Given the ecological significance of microorganisms in algal blooming events, it is critical to understand the mechanisms regarding their distribution under different conditions. We tested the hypothesis that microbial community succession is strongly associated with algal bloom stages, and that the assembly mechanisms are cocontrolled by deterministic and stochastic processes. Community structures and underlying ecological processes of microbial populations (attached and free-living bacteria) at three algal bloom stages (pre-, during, and postbloom) over a complete dinoflagellate Scrippsiella trochoidea bloom were investigated. Both attached and free-living taxa had a strong response to the bloom event, and the latter was more sensitive than the former. The contribution of environmental parameters to microbial variability was 40.2%. Interaction analysis showed that complex positive or negative correlation networks exist in phycosphere microbes. These relationships were the potential drivers of mutualist and competitive interactions that impacted bacterial succession. Null model analysis showed that the attached bacterial community primarily exhibited deterministic processes at pre- and during-bloom stages, while dispersal-related processes contributed to a greater extent at the postbloom stage. In the free-living bacterial community, homogeneous selection and dispersal limitation dominated in the initial phase, which gave way to more deterministic processes at the two later stages. Relative contribution analyses further demonstrated that the community turnover of attached bacteria was mainly driven by environmental selection, while stochastic factors had partial effects on the assembly of free-living bacteria. Taken together, these data demonstrated that a robust link exists between bacterioplankton community structure and bloom progression, and phycosphere microbial succession trajectories are cogoverned by both deterministic and random processes.IMPORTANCE Disentangling the mechanisms shaping bacterioplankton communities during a marine ecological event is a core concern for ecologists. Harmful algal bloom (HAB) is a typical ecological disaster, and its formation is significantly influenced by alga-bacterium interactions. Microbial community shifts during the HAB process are relatively well known. However, the assembly processes of microbial communities in an HAB are not fully understood, especially the relative influences of deterministic and stochastic processes. We therefore analyzed the relative contributions of deterministic and stochastic processes during an HAB event. Both free-living and attached bacterial groups had a dramatic response to the HAB, and the relative importance of determinism versus stochasticity varied between the two bacterial groups at various bloom stages. Environmental factors and biotic interactions were the main drivers impacting the microbial shift process. Our results strengthen the understanding of the ecological mechanisms controlling microbial community patterns during the HAB process.

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Molecular insights into a dinoflagellate bloom.

Publications

Molecular insights into a dinoflagellate bloom.

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