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      Characterization of Potential Polysaccharide Utilization Systems in the Marine Bacteroidetes Gramella Flava JLT2011 Using a Multi-Omics Approach

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          Abstract

          Members of phylum Bacteroidetes are distributed across diverse marine niches and Flavobacteria is often the predominant bacterial class decomposing algae-derived polysaccharides. Here, we report the complete genome of Gramella flava JLT2011 ( Flavobacteria) isolated from surface water of the southeastern Pacific. A remarkable genomic feature is that the number of glycoside hydrolase (GH) genes in the genome of G. flava JLT2011 is more than 2-fold higher than that of other Gramella species. The functional profiles of the GHs suggest extensive variation in Gramella species. Growth experiments revealed that G. flava JLT2011 has the ability to utilize a wide range of polysaccharides for growth such as xylan and homogalacturonan in pectin. Nearly half of all GH genes were located on the multi-gene polysaccharide utilization loci (PUL) or PUL-like systems in G. flava JLT2011. This species was also found to harbor the two xylan PULs and a pectin PUL, respectively. Gene expression data indicated that more GHs and sugar-specific outer-membrane susC-susD systems were found in the presence of xylan than in the presence of pectin, suggesting a different strategy for heteropolymeric xylan and homoglacturonan utilization. Multi-omics data (transcriptomics, proteomics, and metabolomics) indicated that xylan PULs and pectin PUL are respectively involved in the catabolism of their corresponding polysaccharides. This work presents a comparison of polysaccharide decomposition within a genus and expands current knowledge on the diversity and function of PULs in marine Bacteroidetes, thereby deepening our understanding of their ecological role in polysaccharide remineralization in the marine system.

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          Most cited references34

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          Global phytoplankton decline over the past century.

          In the oceans, ubiquitous microscopic phototrophs (phytoplankton) account for approximately half the production of organic matter on Earth. Analyses of satellite-derived phytoplankton concentration (available since 1979) have suggested decadal-scale fluctuations linked to climate forcing, but the length of this record is insufficient to resolve longer-term trends. Here we combine available ocean transparency measurements and in situ chlorophyll observations to estimate the time dependence of phytoplankton biomass at local, regional and global scales since 1899. We observe declines in eight out of ten ocean regions, and estimate a global rate of decline of approximately 1% of the global median per year. Our analyses further reveal interannual to decadal phytoplankton fluctuations superimposed on long-term trends. These fluctuations are strongly correlated with basin-scale climate indices, whereas long-term declining trends are related to increasing sea surface temperatures. We conclude that global phytoplankton concentration has declined over the past century; this decline will need to be considered in future studies of marine ecosystems, geochemical cycling, ocean circulation and fisheries.
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            Bulk chemical characteristics of dissolved organic matter in the ocean.

            Dissolved organic matter (DOM) is the largest reservoir of reduced carbon in the oceans. The nature of DOM is poorly understood, in part, because it has been difficult to isolate sufficient amounts of representative material for analysis. Tangential-flow ultrafiltration was shown to recover milligram amounts of >1000 daltons of DOM from seawater collected at three depths in the North Pacific Ocean. These isolates represented 22 to 33 percent of the total DOM and included essentially all colloidal material. The elemental, carbohydrate, and carbon-type (by (13)C nuclear magnetic resonance) compositions of the isolates indicated that the relative abundance of polysaccharides was high ( approximately 50 percent) in surface water and decreased to approximately 25 percent in deeper samples. Polysaccharides thus appear to be more abundant and reactive components of seawater DOM than has been recognized.
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              Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter.

              We used a method that combines microautoradiography with hybridization of fluorescent rRNA-targeted oligonucleotide probes to whole cells (MICRO-FISH) to test the hypothesis that the relative contributions of various phylogenetic groups to the utilization of dissolved organic matter (DOM) depend solely on their relative abundance in the bacterial community. We found that utilization of even simple low-molecular-weight DOM components by bacteria differed across the major phylogenetic groups and often did not correlate with the relative abundance of these bacterial groups in estuarine and coastal environments. The Cytophaga-Flavobacter cluster was overrepresented in the portion of the assemblage consuming chitin, N-acetylglucosamine, and protein but was generally underrepresented in the assemblage consuming amino acids. The amino acid-consuming assemblage was usually dominated by the alpha subclass of the class Proteobacteria, although the representation of alpha-proteobacteria in the protein-consuming assemblages was about that expected from their relative abundance in the entire bacterial community. In our experiments, no phylogenetic group dominated the consumption of all DOM, suggesting that the participation of a diverse assemblage of bacteria is essential for the complete degradation of complex DOM in the oceans. These results also suggest that the role of aerobic heterotrophic bacteria in carbon cycling would be more accurately described by using three groups instead of the single bacterial compartment currently used in biogeochemical models.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                14 February 2017
                2017
                : 8
                : 220
                Affiliations
                State Key Laboratory for Marine Environmental Science, Institute of Marine Microbes and Ecospheres, Xiamen University Xiamen, China
                Author notes

                Edited by: Rex Malmstrom, DOE Joint Genome Institute, USA

                Reviewed by: Zongze Shao, State Oceanic Administration, China; Thomas Schweder, University of Greifswald, Germany; Fiona Cuskin, Newcastle University, UK

                *Correspondence: Kai Tang tangkai@ 123456xmu.edu.cn

                This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.00220
                5306329
                28261179
                7b2bba42-f741-46e9-b5ef-06ae8e966314
                Copyright © 2017 Tang, Lin, Han and Jiao.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 August 2016
                : 31 January 2017
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 54, Pages: 13, Words: 8661
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Funded by: Natural Science Foundation of Fujian Province 10.13039/501100003392
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                glycoside hydrolases,polysaccharide utilization loci,bacteroidetes,genome,microarray,proteomics,marine bacteria

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