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Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time.

ABSTRACT: Shifts in bacterioplankton community composition along the salinity gradient of the Parker River estuary and Plum Island Sound, in northeastern Massachusetts, were related to residence time and bacterial community doubling time in spring, summer, and fall seasons. Bacterial community composition was characterized with denaturing gradient gel electrophoresis (DGGE) of PCR-amplified 16S ribosomal DNA. Average community doubling time was calculated from bacterial production ([(14)C]leucine incorporation) and bacterial abundance (direct counts). Freshwater and marine populations advected into the estuary represented a large fraction of the bacterioplankton community in all seasons. However, a unique estuarine community formed at intermediate salinities in summer and fall, when average doubling time was much shorter than water residence time, but not in spring, when doubling time was similar to residence time. Sequencing of DNA in DGGE bands demonstrated that most bands represented single phylotypes and that matching bands from different samples represented identical phylotypes. Most river and coastal ocean bacterioplankton were members of common freshwater and marine phylogenetic clusters within the phyla Proteobacteria, Bacteroidetes, and ACTINOBACTERIA: Estuarine bacterioplankton also belonged to these phyla but were related to clones and isolates from several different environments, including marine water columns, freshwater sediments, and soil.

SUBMITTER: Crump BC

PROVIDER: S-EPMC365029 | biostudies-literature | 2004 Mar

REPOSITORIES: biostudies-literature

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Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time.

Crump Byron C BC Hopkinson Charles S CS Sogin Mitchell L ML Hobbie John E JE

Applied and environmental microbiology 20040301 3

Shifts in bacterioplankton community composition along the salinity gradient of the Parker River estuary and Plum Island Sound, in northeastern Massachusetts, were related to residence time and bacterial community doubling time in spring, summer, and fall seasons. Bacterial community composition was characterized with denaturing gradient gel electrophoresis (DGGE) of PCR-amplified 16S ribosomal DNA. Average community doubling time was calculated from bacterial production ([(14)C]leucine incorpor ...[more]

PMID: 15006771

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Project description:BackgroundMicrobial adaptation to salinity has been a classic inquiry in the field of microbiology. It has been demonstrated that microorganisms can endure salinity stress via either the "salt-in" strategy, involving inorganic ion uptake, or the "salt-out" strategy, relying on compatible solutes. While these insights are mostly based on laboratory-cultured isolates, exploring the adaptive mechanisms of microorganisms within natural salinity gradient is crucial for gaining a deeper understanding of microbial adaptation in the estuarine ecosystem.ResultsHere, we conducted metagenomic analyses on filtered surface water samples collected from a typical subtropical short residence-time estuary and categorized them by salinity into low-, intermediate-, and high-salinity metagenomes. Our findings highlighted salinity-driven variations in microbial community composition and function, as revealed through taxonomic and Clusters of Orthologous Group (COG) functional annotations. Through metagenomic binning, 127 bacterial and archaeal metagenome-assembled genomes (MAGs) were reconstructed. These MAGs were categorized as stenohaline-specific to low-, intermediate-, or high-salinity-based on the average relative abundance in one salinity category significantly exceeding those in the other two categories by an order of magnitude. Those that did not meet this criterion were classified as euryhaline, indicating a broader range of salinity tolerance. Applying the Boruta algorithm, a machine learning-based feature selection method, we discerned important genomic features from the stenohaline bacterial MAGs. Of the total 12,162 COGs obtained, 40 were identified as important features, with the "inorganic ion transport and metabolism" COG category emerging as the most prominent. Furthermore, eight COGs were implicated in microbial osmoregulation, of which four were related to the "salt-in" strategy, three to the "salt-out" strategy, and one to the regulation of water channel activity. COG0168, annotated as the Trk-type K+ transporter related to the "salt-in" strategy, was ranked as the most important feature. The relative abundance of COG0168 was observed to increase with rising salinity across metagenomes, the stenohaline strains, and the dominant Actinobacteriota and Proteobacteria phyla.ConclusionsWe demonstrated that salinity exerts influences on both the taxonomic and functional profiles of the microbial communities inhabiting the estuarine ecosystem. Our findings shed light on diverse salinity adaptation strategies employed by the estuarine microbial communities, highlighting the crucial role of the "salt-in" strategy mediated by Trk-type K+ transporters for microorganisms thriving under osmotic stress in the short residence-time estuary. Video Abstract.

Dataset Information

Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time.

Publications

Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time.

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