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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
Main Authors: 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
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creator Kim, Jay W
Brawley, Susan H
Prochnik, Simon
Chovatia, Mansi
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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.
doi_str_mv 10.1371/journal.pone.0151883
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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. 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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, 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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>
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identifier ISSN: 1932-6203
ispartof PloS one, 2016-03, Vol.11 (3), p.e0151883-e0151883
issn 1932-6203
1932-6203
language eng
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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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