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Genome Analysis of Planctomycetes Inhabiting Blades of the Red Alga Porphyra umbilicalis
Porphyra is a macrophytic red alga of the Bangiales that is important ecologically and economically. We describe the genomes of three bacteria in the phylum Planctomycetes (designated P1, P2 and P3) that were isolated from blades of Porphyra umbilicalis (P.um.1). These three Operational Taxonomic Un...
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Published in: | PloS one 2016-03, Vol.11 (3), p.e0151883-e0151883 |
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creator | Kim, Jay W Brawley, Susan H Prochnik, Simon Chovatia, Mansi Grimwood, Jane Jenkins, Jerry LaButti, Kurt Mavromatis, Konstantinos Nolan, Matt Zane, Matthew Schmutz, Jeremy Stiller, John W Grossman, Arthur R |
description | Porphyra is a macrophytic red alga of the Bangiales that is important ecologically and economically. We describe the genomes of three bacteria in the phylum Planctomycetes (designated P1, P2 and P3) that were isolated from blades of Porphyra umbilicalis (P.um.1). These three Operational Taxonomic Units (OTUs) belong to distinct genera; P2 belongs to the genus Rhodopirellula, while P1 and P3 represent undescribed genera within the Planctomycetes. Comparative analyses of the P1, P2 and P3 genomes show large expansions of distinct gene families, which can be widespread throughout the Planctomycetes (e.g., protein kinases, sensors/response regulators) and may relate to specific habitat (e.g., sulfatase gene expansions in marine Planctomycetes) or phylogenetic position. Notably, there are major differences among the Planctomycetes in the numbers and sub-functional diversity of enzymes (e.g., sulfatases, glycoside hydrolases, polysaccharide lyases) that allow these bacteria to access a range of sulfated polysaccharides in macroalgal cell walls. These differences suggest that the microbes have varied capacities for feeding on fixed carbon in the cell walls of P.um.1 and other macrophytic algae, although the activities among the various bacteria might be functionally complementary in situ. Additionally, phylogenetic analyses indicate augmentation of gene functions through expansions arising from gene duplications and horizontal gene transfers; examples include genes involved in cell wall degradation (e.g., κ-carrageenase, alginate lyase, fucosidase) and stress responses (e.g., efflux pump, amino acid transporter). Finally P1 and P2 contain various genes encoding selenoproteins, many of which are enzymes that ameliorate the impact of environmental stresses that occur in the intertidal habitat. |
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We describe the genomes of three bacteria in the phylum Planctomycetes (designated P1, P2 and P3) that were isolated from blades of Porphyra umbilicalis (P.um.1). These three Operational Taxonomic Units (OTUs) belong to distinct genera; P2 belongs to the genus Rhodopirellula, while P1 and P3 represent undescribed genera within the Planctomycetes. Comparative analyses of the P1, P2 and P3 genomes show large expansions of distinct gene families, which can be widespread throughout the Planctomycetes (e.g., protein kinases, sensors/response regulators) and may relate to specific habitat (e.g., sulfatase gene expansions in marine Planctomycetes) or phylogenetic position. Notably, there are major differences among the Planctomycetes in the numbers and sub-functional diversity of enzymes (e.g., sulfatases, glycoside hydrolases, polysaccharide lyases) that allow these bacteria to access a range of sulfated polysaccharides in macroalgal cell walls. These differences suggest that the microbes have varied capacities for feeding on fixed carbon in the cell walls of P.um.1 and other macrophytic algae, although the activities among the various bacteria might be functionally complementary in situ. Additionally, phylogenetic analyses indicate augmentation of gene functions through expansions arising from gene duplications and horizontal gene transfers; examples include genes involved in cell wall degradation (e.g., κ-carrageenase, alginate lyase, fucosidase) and stress responses (e.g., efflux pump, amino acid transporter). Finally P1 and P2 contain various genes encoding selenoproteins, many of which are enzymes that ameliorate the impact of environmental stresses that occur in the intertidal habitat.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0151883</identifier><identifier>PMID: 27015628</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abiotic stress ; Algae ; Alginate lyase ; Alginic acid ; Amino acids ; Analysis ; Augmentation ; Bacteria ; Bacteroidetes ; BASIC BIOLOGICAL SCIENCES ; Biodegradation ; Biology and Life Sciences ; Blades ; Cell walls ; Cellulose ; Chlorophyta ; Computer and Information Sciences ; Ecology ; Efflux ; Environmental impact ; Environmental stress ; Enzymes ; Evolution ; Gene families ; Gene Transfer, Horizontal ; Genera ; Genes ; Genome, Bacterial ; Genomes ; Genomics ; Glycoside hydrolase ; Kinases ; Laboratories ; National parks ; Phaeophyceae ; Phylogenetics ; Phylogeny ; Planctomycetales - genetics ; Planctomycetes ; Polysaccharides ; Porphyra ; Porphyra - genetics ; Porphyra - microbiology ; Porphyra umbilicalis ; Protein kinase ; Proteins ; Proteobacteria ; Red algae ; Regulators ; Research and Analysis Methods ; Rhodophyta ; Saccharides ; Seaweeds ; Selenium ; Selenoproteins ; Sulfatases - genetics ; Transporter</subject><ispartof>PloS one, 2016-03, Vol.11 (3), p.e0151883-e0151883</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c719t-1614217f60ce786253a47b51a42053744cb657a3e789896e300dcea45497d5183</citedby><cites>FETCH-LOGICAL-c719t-1614217f60ce786253a47b51a42053744cb657a3e789896e300dcea45497d5183</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1775975387/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1775975387?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768,74869</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27015628$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1615260$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><contributor>Pombert, Jean-François</contributor><creatorcontrib>Kim, Jay W</creatorcontrib><creatorcontrib>Brawley, Susan H</creatorcontrib><creatorcontrib>Prochnik, Simon</creatorcontrib><creatorcontrib>Chovatia, Mansi</creatorcontrib><creatorcontrib>Grimwood, Jane</creatorcontrib><creatorcontrib>Jenkins, Jerry</creatorcontrib><creatorcontrib>LaButti, Kurt</creatorcontrib><creatorcontrib>Mavromatis, Konstantinos</creatorcontrib><creatorcontrib>Nolan, Matt</creatorcontrib><creatorcontrib>Zane, Matthew</creatorcontrib><creatorcontrib>Schmutz, Jeremy</creatorcontrib><creatorcontrib>Stiller, John W</creatorcontrib><creatorcontrib>Grossman, Arthur R</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><title>Genome Analysis of Planctomycetes Inhabiting Blades of the Red Alga Porphyra umbilicalis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Porphyra is a macrophytic red alga of the Bangiales that is important ecologically and economically. We describe the genomes of three bacteria in the phylum Planctomycetes (designated P1, P2 and P3) that were isolated from blades of Porphyra umbilicalis (P.um.1). These three Operational Taxonomic Units (OTUs) belong to distinct genera; P2 belongs to the genus Rhodopirellula, while P1 and P3 represent undescribed genera within the Planctomycetes. Comparative analyses of the P1, P2 and P3 genomes show large expansions of distinct gene families, which can be widespread throughout the Planctomycetes (e.g., protein kinases, sensors/response regulators) and may relate to specific habitat (e.g., sulfatase gene expansions in marine Planctomycetes) or phylogenetic position. Notably, there are major differences among the Planctomycetes in the numbers and sub-functional diversity of enzymes (e.g., sulfatases, glycoside hydrolases, polysaccharide lyases) that allow these bacteria to access a range of sulfated polysaccharides in macroalgal cell walls. These differences suggest that the microbes have varied capacities for feeding on fixed carbon in the cell walls of P.um.1 and other macrophytic algae, although the activities among the various bacteria might be functionally complementary in situ. Additionally, phylogenetic analyses indicate augmentation of gene functions through expansions arising from gene duplications and horizontal gene transfers; examples include genes involved in cell wall degradation (e.g., κ-carrageenase, alginate lyase, fucosidase) and stress responses (e.g., efflux pump, amino acid transporter). Finally P1 and P2 contain various genes encoding selenoproteins, many of which are enzymes that ameliorate the impact of environmental stresses that occur in the intertidal habitat.</description><subject>Abiotic stress</subject><subject>Algae</subject><subject>Alginate lyase</subject><subject>Alginic acid</subject><subject>Amino acids</subject><subject>Analysis</subject><subject>Augmentation</subject><subject>Bacteria</subject><subject>Bacteroidetes</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biodegradation</subject><subject>Biology and Life Sciences</subject><subject>Blades</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Chlorophyta</subject><subject>Computer and Information Sciences</subject><subject>Ecology</subject><subject>Efflux</subject><subject>Environmental impact</subject><subject>Environmental stress</subject><subject>Enzymes</subject><subject>Evolution</subject><subject>Gene families</subject><subject>Gene Transfer, Horizontal</subject><subject>Genera</subject><subject>Genes</subject><subject>Genome, Bacterial</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Glycoside hydrolase</subject><subject>Kinases</subject><subject>Laboratories</subject><subject>National parks</subject><subject>Phaeophyceae</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Planctomycetales - genetics</subject><subject>Planctomycetes</subject><subject>Polysaccharides</subject><subject>Porphyra</subject><subject>Porphyra - genetics</subject><subject>Porphyra - microbiology</subject><subject>Porphyra umbilicalis</subject><subject>Protein kinase</subject><subject>Proteins</subject><subject>Proteobacteria</subject><subject>Red algae</subject><subject>Regulators</subject><subject>Research and Analysis Methods</subject><subject>Rhodophyta</subject><subject>Saccharides</subject><subject>Seaweeds</subject><subject>Selenium</subject><subject>Selenoproteins</subject><subject>Sulfatases 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Analysis of Planctomycetes Inhabiting Blades of the Red Alga Porphyra umbilicalis</title><author>Kim, Jay W ; Brawley, Susan H ; Prochnik, Simon ; Chovatia, Mansi ; Grimwood, Jane ; Jenkins, Jerry ; LaButti, Kurt ; Mavromatis, Konstantinos ; Nolan, Matt ; Zane, Matthew ; Schmutz, Jeremy ; Stiller, John W ; Grossman, Arthur R</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c719t-1614217f60ce786253a47b51a42053744cb657a3e789896e300dcea45497d5183</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Abiotic stress</topic><topic>Algae</topic><topic>Alginate lyase</topic><topic>Alginic acid</topic><topic>Amino acids</topic><topic>Analysis</topic><topic>Augmentation</topic><topic>Bacteria</topic><topic>Bacteroidetes</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biodegradation</topic><topic>Biology and Life Sciences</topic><topic>Blades</topic><topic>Cell 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Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kim, Jay W</au><au>Brawley, Susan H</au><au>Prochnik, Simon</au><au>Chovatia, Mansi</au><au>Grimwood, Jane</au><au>Jenkins, Jerry</au><au>LaButti, Kurt</au><au>Mavromatis, Konstantinos</au><au>Nolan, Matt</au><au>Zane, Matthew</au><au>Schmutz, Jeremy</au><au>Stiller, John W</au><au>Grossman, Arthur R</au><au>Pombert, Jean-François</au><aucorp>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome Analysis of Planctomycetes Inhabiting Blades of the Red Alga Porphyra umbilicalis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-03-25</date><risdate>2016</risdate><volume>11</volume><issue>3</issue><spage>e0151883</spage><epage>e0151883</epage><pages>e0151883-e0151883</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Porphyra is a macrophytic red alga of the Bangiales that is important ecologically and economically. We describe the genomes of three bacteria in the phylum Planctomycetes (designated P1, P2 and P3) that were isolated from blades of Porphyra umbilicalis (P.um.1). These three Operational Taxonomic Units (OTUs) belong to distinct genera; P2 belongs to the genus Rhodopirellula, while P1 and P3 represent undescribed genera within the Planctomycetes. Comparative analyses of the P1, P2 and P3 genomes show large expansions of distinct gene families, which can be widespread throughout the Planctomycetes (e.g., protein kinases, sensors/response regulators) and may relate to specific habitat (e.g., sulfatase gene expansions in marine Planctomycetes) or phylogenetic position. Notably, there are major differences among the Planctomycetes in the numbers and sub-functional diversity of enzymes (e.g., sulfatases, glycoside hydrolases, polysaccharide lyases) that allow these bacteria to access a range of sulfated polysaccharides in macroalgal cell walls. These differences suggest that the microbes have varied capacities for feeding on fixed carbon in the cell walls of P.um.1 and other macrophytic algae, although the activities among the various bacteria might be functionally complementary in situ. Additionally, phylogenetic analyses indicate augmentation of gene functions through expansions arising from gene duplications and horizontal gene transfers; examples include genes involved in cell wall degradation (e.g., κ-carrageenase, alginate lyase, fucosidase) and stress responses (e.g., efflux pump, amino acid transporter). Finally P1 and P2 contain various genes encoding selenoproteins, many of which are enzymes that ameliorate the impact of environmental stresses that occur in the intertidal habitat.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27015628</pmid><doi>10.1371/journal.pone.0151883</doi><tpages>e0151883</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2016-03, Vol.11 (3), p.e0151883-e0151883 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1775975387 |
source | Publicly Available Content Database; PubMed Central |
subjects | Abiotic stress Algae Alginate lyase Alginic acid Amino acids Analysis Augmentation Bacteria Bacteroidetes BASIC BIOLOGICAL SCIENCES Biodegradation Biology and Life Sciences Blades Cell walls Cellulose Chlorophyta Computer and Information Sciences Ecology Efflux Environmental impact Environmental stress Enzymes Evolution Gene families Gene Transfer, Horizontal Genera Genes Genome, Bacterial Genomes Genomics Glycoside hydrolase Kinases Laboratories National parks Phaeophyceae Phylogenetics Phylogeny Planctomycetales - genetics Planctomycetes Polysaccharides Porphyra Porphyra - genetics Porphyra - microbiology Porphyra umbilicalis Protein kinase Proteins Proteobacteria Red algae Regulators Research and Analysis Methods Rhodophyta Saccharides Seaweeds Selenium Selenoproteins Sulfatases - genetics Transporter |
title | Genome Analysis of Planctomycetes Inhabiting Blades of the Red Alga Porphyra umbilicalis |
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