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Organic Particles: Heterogeneous Hubs for Microbial Interactions in Aquatic Ecosystems

  • The dynamics and activities of microbes colonizing organic particles (hereafter particles) greatly determine the efficiency of the aquatic carbon pump. Current understanding is that particle composition, structure and surface properties, determined mostly by the forming organisms and organic matter, dictate initial microbial colonization and the subsequent rapid succession events taking place as organic matter lability and nutrient content change with microbial degradation. We applied a transcriptomic approach to assess the role of stochastic events on initial microbial colonization of particles. Furthermore, we asked whether gene expression corroborates rapid changes in carbon-quality. Commonly used size fractionated filtration averages thousands of particles of different sizes, sources, and ages. To overcome this drawback, we used replicate samples consisting each of 3–4 particles of identical source and age and further evaluated the consequences of averaging 10–1000s of particles. Using flow-through rolling tanks we conductedThe dynamics and activities of microbes colonizing organic particles (hereafter particles) greatly determine the efficiency of the aquatic carbon pump. Current understanding is that particle composition, structure and surface properties, determined mostly by the forming organisms and organic matter, dictate initial microbial colonization and the subsequent rapid succession events taking place as organic matter lability and nutrient content change with microbial degradation. We applied a transcriptomic approach to assess the role of stochastic events on initial microbial colonization of particles. Furthermore, we asked whether gene expression corroborates rapid changes in carbon-quality. Commonly used size fractionated filtration averages thousands of particles of different sizes, sources, and ages. To overcome this drawback, we used replicate samples consisting each of 3–4 particles of identical source and age and further evaluated the consequences of averaging 10–1000s of particles. Using flow-through rolling tanks we conducted long-term experiments at near in situ conditions minimizing the biasing effects of closed incubation approaches often referred to as “the bottle-effect.” In our open flow-through rolling tank system, however, active microbial communities were highly heterogeneous despite an identical particle source, suggesting random initial colonization. Contrasting previous reports using closed incubation systems, expression of carbon utilization genes didn’t change after 1 week of incubation. Consequently, we suggest that in nature, changes in particle-associated community related to carbon availability are much slower (days to weeks) due to constant supply of labile, easily degradable organic matter. Initial, random particle colonization seems to be subsequently altered by multiple organismic interactions shaping microbial community interactions and functional dynamics. Comparative analysis of thousands particles pooled togethers as well as pooled samples suggests that mechanistic studies of microbial dynamics should be done on single particles. The observed microbial heterogeneity and inter-organismic interactions may have important implications for evolution and biogeochemistry in aquatic systems.show moreshow less

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Author details:Mina Bizic-Ionescu, Danny IonescuORCiD, Hans-Peter GrossartORCiDGND
DOI:https://doi.org/10.3389/fmicb.2018.02569
ISSN:1664-302X
Pubmed ID:https://pubmed.ncbi.nlm.nih.gov/30416497
Title of parent work (English):Frontiers in microbiology
Publisher:Frontiers Research Foundation
Place of publishing:Lausanne
Publication type:Article
Language:English
Date of first publication:2018/10/26
Publication year:2018
Release date:2021/07/26
Tag:antagonism; inter- and intra-species interactions; microbial communities; particle-associated bacteria; phage; transcriptome
Volume:9
Number of pages:15
Funding institution:Leibniz Society; German Science Foundation (DFG)German Research Foundation (DFG) [GR 1540/21-1, GR 1540/23-1]; German Academic Exchange Service DAADDeutscher Akademischer Austausch Dienst (DAAD)
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
DDC classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Peer review:Referiert
Publishing method:Open Access / Gold Open-Access
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License (German):License LogoCC-BY - Namensnennung 4.0 International
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