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Phycosphere Microbial Succession Patterns and Assembly Mechanisms in a Marine Dinoflagellate Bloom.

ABSTRACT: 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.

SUBMITTER: Zhou J

PROVIDER: S-EPMC6643250 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Phycosphere Microbial Succession Patterns and Assembly Mechanisms in a Marine Dinoflagellate Bloom.

Zhou Jin J Chen Guo-Fu GF Ying Ke-Zhen KZ Jin Hui H Song Jun-Ting JT Cai Zhong-Hua ZH

Applied and environmental microbiology 20190718 15

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) a ...[more]

PMID: 31126952

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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:Although the importance of microbiota in the natural environment and in industrial production has been widely recognized, little is known about the formation and succession patterns of the microbial community, particularly secondary succession after disturbance. Here, we choose the Xiaoqu liquor brewing process as an experimental model in which sorghum grains were first aerobically saccharified and then anaerobically fermented after being stirred and acidified to explore multistage community succession patterns. We analyzed microbial composition, physicochemical factors, and metabolites of brewing grains inoculated with two different starters, pure starter and traditional starter, respectively. Two groups showed similar succession patterns where the saccharification microbiota was mainly derived from starters, while environmental microorganisms, mainly Lactobacillaceae and Saccharomyces, dominated the fermentation microbiota regardless of the original saccharification community composition. Species replacement shaped the bacterial community, while species replacement and loss both contributed to fungal community succession in both groups. Grain acidification and hypoxia led to the succession of bacterial and fungal communities during fermentation, respectively. Despite inoculation with starters containing different microorganisms, similar microbial communities during the fermentation stage of the two groups exhibited similar metabolite composition. However, higher abundance of Rhizopus in the saccharification of the pure starter group led to more alcohols, while higher abundance of Monascus and Saccharomycopsis in the traditional starter group promoted acid and ester metabolism. These results revealed the microbial succession patterns of two-stage liquor brewing and its influence on flavor metabolism, which could be used to regulate the microbial community in food fermentation to further promote the modernization of the fermented food industry. IMPORTANCE Revealing formation and assembly mechanisms of microbiota can help us to understand and further regulate its roles in the ecosystems. The Xiaoqu liquor brewing system is a tractable microbial ecosystem with low complexity. This two-stage microbial ecosystem can be used as an experimental model to analyze the multistage temporal succession pattern of microbial communities. Our results demonstrated the dynamic composition and succession pattern of a microbial community in the two-stage liquor brewing system. The results also revealed the microbial origins determining community composition, the ecological processes dominating microbial community succession patterns, the determinants affecting microbial community successions, and the effect of microbial community changes on metabolite synthesis. Overall, our study not only provides an insight into multistage succession patterns of microbial communities in liquor brewing systems but also provides reference for optimizing the quality of fermented products, which will be helpful to understand the succession patterns of microbial communities in other natural ecosystems.

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Phycosphere Microbial Succession Patterns and Assembly Mechanisms in a Marine Dinoflagellate Bloom.

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Phycosphere Microbial Succession Patterns and Assembly Mechanisms in a Marine Dinoflagellate Bloom.

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