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Culture-independent characterization of novel psychrophilic magnetotactic cocci from Antarctic marine sediments

Summary Magnetotactic bacteria (MTB) are a heterogeneous group of ubiquitous aquatic microorganisms capable of biomineralizing nano‐sized, membrane‐bound, magnetic iron‐rich mineral particles called magnetosomes. MTB are found in chemically‐stratified aquatic sediments and/or water columns with a wi...

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Published in:Environmental microbiology 2016-12, Vol.18 (12), p.4426-4441
Main Authors: Abreu, Fernanda, Carolina, Ana, Araujo, V., Leão, Pedro, Silva, Karen Tavares, Carvalho, Fabíola Marques de, Cunha, Oberdan de Lima, Almeida, Luiz Gonzaga, Geurink, Corey, Farina, Marcos, Rodelli, Daniel, Jovane, Luigi, Pellizari, Vivian H., Vasconcelos, Ana Tereza de, Bazylinski, Dennis A., Lins, Ulysses
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cited_by cdi_FETCH-LOGICAL-c4428-1cb0813fff19186e9755135b90446de8676f95896b51a17d96bc66f6f35da8dc3
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container_end_page 4441
container_issue 12
container_start_page 4426
container_title Environmental microbiology
container_volume 18
creator Abreu, Fernanda
Carolina, Ana
Araujo, V.
Leão, Pedro
Silva, Karen Tavares
Carvalho, Fabíola Marques de
Cunha, Oberdan de Lima
Almeida, Luiz Gonzaga
Geurink, Corey
Farina, Marcos
Rodelli, Daniel
Jovane, Luigi
Pellizari, Vivian H.
Vasconcelos, Ana Tereza de
Bazylinski, Dennis A.
Lins, Ulysses
description Summary Magnetotactic bacteria (MTB) are a heterogeneous group of ubiquitous aquatic microorganisms capable of biomineralizing nano‐sized, membrane‐bound, magnetic iron‐rich mineral particles called magnetosomes. MTB are found in chemically‐stratified aquatic sediments and/or water columns with a wide range of salinities, moderate to high temperatures, and pH varying from neutral to strongly alkaline. MTB from very cold environments have not been investigated to any great degree and here we characterize MTB from the low temperature Antarctic maritime region. Sediment samples were collected at nine sampling sites within Admiralty Bay, King George Island (62°23′S 58°27′W) from 2009 to 2013. Samples from five sites contained MTB and those from two of these sites contained large number of magnetotactic cocci that were studied using electron microscopy and molecular techniques. The magnetotactic cocci contained magnetosomes either arranged as two or four chains or as a disorganized cluster. The crystalline habit and composition of all magnetosomes analyzed with high‐resolution transmission electron microscopy and energy dispersive X‐ray microanalysis were consistent with elongated prismatic crystals of magnetite (Fe3O4). The retrieved 16S rRNA gene sequences from magnetically‐enriched magnetotactic cocci clustered into three distinct groups affiliated with the Alphaproteobacteria class of the Proteobacteria. Novel sequences of each phylogenetic cluster were confirmed using fluorescent in situ hybridization. Metagenomic data analysis of magnetically‐enriched magnetotactic cocci revealed the presence of mam genes and MTB‐specific hypothetical protein coding genes. Sequence homology and phylogenetic analysis indicated that predicted proteins are related to those of cultivated alphaproteobacterial MTB. The consistent and continuous low temperature of the sediment where the magnetotactic cocci are present (always below 1°C) suggests that these MTB from maritime Antarctica are psychrophiles. Moreover, similar morphotypes and 16S gene sequences were retrieved from samples collected from different sites from maritime Antarctica for several years suggesting that these new strains of MTB are indigenous members of Antarctic microbiota.
doi_str_mv 10.1111/1462-2920.13388
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MTB are found in chemically‐stratified aquatic sediments and/or water columns with a wide range of salinities, moderate to high temperatures, and pH varying from neutral to strongly alkaline. MTB from very cold environments have not been investigated to any great degree and here we characterize MTB from the low temperature Antarctic maritime region. Sediment samples were collected at nine sampling sites within Admiralty Bay, King George Island (62°23′S 58°27′W) from 2009 to 2013. Samples from five sites contained MTB and those from two of these sites contained large number of magnetotactic cocci that were studied using electron microscopy and molecular techniques. The magnetotactic cocci contained magnetosomes either arranged as two or four chains or as a disorganized cluster. The crystalline habit and composition of all magnetosomes analyzed with high‐resolution transmission electron microscopy and energy dispersive X‐ray microanalysis were consistent with elongated prismatic crystals of magnetite (Fe3O4). The retrieved 16S rRNA gene sequences from magnetically‐enriched magnetotactic cocci clustered into three distinct groups affiliated with the Alphaproteobacteria class of the Proteobacteria. Novel sequences of each phylogenetic cluster were confirmed using fluorescent in situ hybridization. Metagenomic data analysis of magnetically‐enriched magnetotactic cocci revealed the presence of mam genes and MTB‐specific hypothetical protein coding genes. Sequence homology and phylogenetic analysis indicated that predicted proteins are related to those of cultivated alphaproteobacterial MTB. The consistent and continuous low temperature of the sediment where the magnetotactic cocci are present (always below 1°C) suggests that these MTB from maritime Antarctica are psychrophiles. Moreover, similar morphotypes and 16S gene sequences were retrieved from samples collected from different sites from maritime Antarctica for several years suggesting that these new strains of MTB are indigenous members of Antarctic microbiota.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.13388</identifier><identifier>PMID: 27241114</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Alphaproteobacteria - classification ; Alphaproteobacteria - genetics ; Alphaproteobacteria - growth &amp; development ; Alphaproteobacteria - isolation &amp; purification ; Antarctic Regions ; Culture Media - chemistry ; Culture Media - metabolism ; DNA, Bacterial - genetics ; Geologic Sediments - chemistry ; Geologic Sediments - microbiology ; In Situ Hybridization, Fluorescence ; Magnetosomes ; Microscopy, Electron, Transmission ; Phylogeny ; Proteobacteria ; RNA, Ribosomal, 16S - genetics ; Salinity ; Seawater - chemistry ; Seawater - microbiology</subject><ispartof>Environmental microbiology, 2016-12, Vol.18 (12), p.4426-4441</ispartof><rights>2016 Society for Applied Microbiology and John Wiley &amp; Sons Ltd</rights><rights>2016 Society for Applied Microbiology and John Wiley &amp; Sons Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4428-1cb0813fff19186e9755135b90446de8676f95896b51a17d96bc66f6f35da8dc3</citedby><cites>FETCH-LOGICAL-c4428-1cb0813fff19186e9755135b90446de8676f95896b51a17d96bc66f6f35da8dc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27241114$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Abreu, Fernanda</creatorcontrib><creatorcontrib>Carolina, Ana</creatorcontrib><creatorcontrib>Araujo, V.</creatorcontrib><creatorcontrib>Leão, Pedro</creatorcontrib><creatorcontrib>Silva, Karen Tavares</creatorcontrib><creatorcontrib>Carvalho, Fabíola Marques de</creatorcontrib><creatorcontrib>Cunha, Oberdan de Lima</creatorcontrib><creatorcontrib>Almeida, Luiz Gonzaga</creatorcontrib><creatorcontrib>Geurink, Corey</creatorcontrib><creatorcontrib>Farina, Marcos</creatorcontrib><creatorcontrib>Rodelli, Daniel</creatorcontrib><creatorcontrib>Jovane, Luigi</creatorcontrib><creatorcontrib>Pellizari, Vivian H.</creatorcontrib><creatorcontrib>Vasconcelos, Ana Tereza de</creatorcontrib><creatorcontrib>Bazylinski, Dennis A.</creatorcontrib><creatorcontrib>Lins, Ulysses</creatorcontrib><title>Culture-independent characterization of novel psychrophilic magnetotactic cocci from Antarctic marine sediments</title><title>Environmental microbiology</title><addtitle>Environmental Microbiology</addtitle><description>Summary Magnetotactic bacteria (MTB) are a heterogeneous group of ubiquitous aquatic microorganisms capable of biomineralizing nano‐sized, membrane‐bound, magnetic iron‐rich mineral particles called magnetosomes. MTB are found in chemically‐stratified aquatic sediments and/or water columns with a wide range of salinities, moderate to high temperatures, and pH varying from neutral to strongly alkaline. MTB from very cold environments have not been investigated to any great degree and here we characterize MTB from the low temperature Antarctic maritime region. Sediment samples were collected at nine sampling sites within Admiralty Bay, King George Island (62°23′S 58°27′W) from 2009 to 2013. Samples from five sites contained MTB and those from two of these sites contained large number of magnetotactic cocci that were studied using electron microscopy and molecular techniques. The magnetotactic cocci contained magnetosomes either arranged as two or four chains or as a disorganized cluster. The crystalline habit and composition of all magnetosomes analyzed with high‐resolution transmission electron microscopy and energy dispersive X‐ray microanalysis were consistent with elongated prismatic crystals of magnetite (Fe3O4). The retrieved 16S rRNA gene sequences from magnetically‐enriched magnetotactic cocci clustered into three distinct groups affiliated with the Alphaproteobacteria class of the Proteobacteria. Novel sequences of each phylogenetic cluster were confirmed using fluorescent in situ hybridization. Metagenomic data analysis of magnetically‐enriched magnetotactic cocci revealed the presence of mam genes and MTB‐specific hypothetical protein coding genes. Sequence homology and phylogenetic analysis indicated that predicted proteins are related to those of cultivated alphaproteobacterial MTB. The consistent and continuous low temperature of the sediment where the magnetotactic cocci are present (always below 1°C) suggests that these MTB from maritime Antarctica are psychrophiles. 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MTB are found in chemically‐stratified aquatic sediments and/or water columns with a wide range of salinities, moderate to high temperatures, and pH varying from neutral to strongly alkaline. MTB from very cold environments have not been investigated to any great degree and here we characterize MTB from the low temperature Antarctic maritime region. Sediment samples were collected at nine sampling sites within Admiralty Bay, King George Island (62°23′S 58°27′W) from 2009 to 2013. Samples from five sites contained MTB and those from two of these sites contained large number of magnetotactic cocci that were studied using electron microscopy and molecular techniques. The magnetotactic cocci contained magnetosomes either arranged as two or four chains or as a disorganized cluster. The crystalline habit and composition of all magnetosomes analyzed with high‐resolution transmission electron microscopy and energy dispersive X‐ray microanalysis were consistent with elongated prismatic crystals of magnetite (Fe3O4). The retrieved 16S rRNA gene sequences from magnetically‐enriched magnetotactic cocci clustered into three distinct groups affiliated with the Alphaproteobacteria class of the Proteobacteria. Novel sequences of each phylogenetic cluster were confirmed using fluorescent in situ hybridization. Metagenomic data analysis of magnetically‐enriched magnetotactic cocci revealed the presence of mam genes and MTB‐specific hypothetical protein coding genes. Sequence homology and phylogenetic analysis indicated that predicted proteins are related to those of cultivated alphaproteobacterial MTB. The consistent and continuous low temperature of the sediment where the magnetotactic cocci are present (always below 1°C) suggests that these MTB from maritime Antarctica are psychrophiles. Moreover, similar morphotypes and 16S gene sequences were retrieved from samples collected from different sites from maritime Antarctica for several years suggesting that these new strains of MTB are indigenous members of Antarctic microbiota.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>27241114</pmid><doi>10.1111/1462-2920.13388</doi><tpages>16</tpages></addata></record>
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subjects Alphaproteobacteria - classification
Alphaproteobacteria - genetics
Alphaproteobacteria - growth & development
Alphaproteobacteria - isolation & purification
Antarctic Regions
Culture Media - chemistry
Culture Media - metabolism
DNA, Bacterial - genetics
Geologic Sediments - chemistry
Geologic Sediments - microbiology
In Situ Hybridization, Fluorescence
Magnetosomes
Microscopy, Electron, Transmission
Phylogeny
Proteobacteria
RNA, Ribosomal, 16S - genetics
Salinity
Seawater - chemistry
Seawater - microbiology
title Culture-independent characterization of novel psychrophilic magnetotactic cocci from Antarctic marine sediments
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