Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress
Seagrasses thrive in anoxic sediments where sulphide can accumulate to phytotoxic levels. So how do seagrasses persist in this environment? Here, we propose that radial oxygen loss (ROL) from actively growing root tips protects seagrasses from sulphide intrusion not only by abiotically oxidising sul...
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description | Seagrasses thrive in anoxic sediments where sulphide can accumulate to phytotoxic levels. So how do seagrasses persist in this environment? Here, we propose that radial oxygen loss (ROL) from actively growing root tips protects seagrasses from sulphide intrusion not only by abiotically oxidising sulphides in the rhizosphere of young roots, but also by influencing the abundance and spatial distribution of sulphate-reducing and sulphide-oxidising bacteria. We used a novel multifaceted approach combining imaging techniques (confocal fluorescence in situ hybridisation, oxygen planar optodes, and sulphide diffusive gradients in thin films) with microbial community profiling to build a complete picture of the microenvironment of growing roots of the seagrasses
Halophila ovalis
and
Zostera muelleri
. ROL was restricted to young root tips, indicating that seagrasses will have limited ability to influence sulphide oxidation in bulk sediments. On the microscale, however, ROL corresponded with decreased abundance of potential sulphate-reducing bacteria and decreased sulphide concentrations in the rhizosphere surrounding young roots. Furthermore, roots leaking oxygen had a higher abundance of sulphide-oxidising cable bacteria; which is the first direct observation of these bacteria on seagrass roots. Thus, ROL may enhance both abiotic and bacterial sulphide oxidation and restrict bacterial sulphide production around vulnerable roots, thereby helping seagrasses to colonise sulphide-rich anoxic sediments. |
doi_str_mv | 10.1038/s41396-018-0308-5 |
format | Article |
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Halophila ovalis
and
Zostera muelleri
. ROL was restricted to young root tips, indicating that seagrasses will have limited ability to influence sulphide oxidation in bulk sediments. On the microscale, however, ROL corresponded with decreased abundance of potential sulphate-reducing bacteria and decreased sulphide concentrations in the rhizosphere surrounding young roots. Furthermore, roots leaking oxygen had a higher abundance of sulphide-oxidising cable bacteria; which is the first direct observation of these bacteria on seagrass roots. Thus, ROL may enhance both abiotic and bacterial sulphide oxidation and restrict bacterial sulphide production around vulnerable roots, thereby helping seagrasses to colonise sulphide-rich anoxic sediments.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/s41396-018-0308-5</identifier><identifier>PMID: 30353038</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14/19 ; 14/32 ; 14/34 ; 14/63 ; 38/23 ; 38/77 ; 631/326/171 ; 631/449/2668 ; Abundance ; Bacteria ; Bacteria - classification ; Bacteria - genetics ; Bacteria - metabolism ; Biodiversity ; Biomedical and Life Sciences ; Ecology ; Evolutionary Biology ; Fluorescence ; Geologic Sediments - chemistry ; Grasses ; Hybridization ; Hydrocharitaceae - microbiology ; Hydrocharitaceae - physiology ; Imaging techniques ; Intrusion ; Life Sciences ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microorganisms ; Oxidation ; Oxidation-Reduction ; Oxygen ; Oxygen - metabolism ; Plant Roots - microbiology ; Plant Roots - physiology ; Protective coatings ; Rhizosphere ; Roots ; Seagrasses ; Sediments ; Spatial distribution ; Stress, Physiological ; Sulfate reduction ; Sulfate-reducing bacteria ; Sulfates ; Sulfides ; Sulfides - metabolism ; Thin films ; Tips ; Zosteraceae - microbiology ; Zosteraceae - physiology</subject><ispartof>The ISME Journal, 2019-03, Vol.13 (3), p.707-719</ispartof><rights>International Society for Microbial Ecology 2018</rights><rights>Copyright Nature Publishing Group Mar 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-c9d374420f3ed582c49739eab23c1a2c6a466f33c438036ef6dc7591d2b4e3b93</citedby><cites>FETCH-LOGICAL-c470t-c9d374420f3ed582c49739eab23c1a2c6a466f33c438036ef6dc7591d2b4e3b93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6461758/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6461758/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30353038$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Martin, Belinda C.</creatorcontrib><creatorcontrib>Bougoure, Jeremy</creatorcontrib><creatorcontrib>Ryan, Megan H.</creatorcontrib><creatorcontrib>Bennett, William W.</creatorcontrib><creatorcontrib>Colmer, Timothy D.</creatorcontrib><creatorcontrib>Joyce, Natalie K.</creatorcontrib><creatorcontrib>Olsen, Ylva S.</creatorcontrib><creatorcontrib>Kendrick, Gary A.</creatorcontrib><title>Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Seagrasses thrive in anoxic sediments where sulphide can accumulate to phytotoxic levels. So how do seagrasses persist in this environment? Here, we propose that radial oxygen loss (ROL) from actively growing root tips protects seagrasses from sulphide intrusion not only by abiotically oxidising sulphides in the rhizosphere of young roots, but also by influencing the abundance and spatial distribution of sulphate-reducing and sulphide-oxidising bacteria. We used a novel multifaceted approach combining imaging techniques (confocal fluorescence in situ hybridisation, oxygen planar optodes, and sulphide diffusive gradients in thin films) with microbial community profiling to build a complete picture of the microenvironment of growing roots of the seagrasses
Halophila ovalis
and
Zostera muelleri
. ROL was restricted to young root tips, indicating that seagrasses will have limited ability to influence sulphide oxidation in bulk sediments. On the microscale, however, ROL corresponded with decreased abundance of potential sulphate-reducing bacteria and decreased sulphide concentrations in the rhizosphere surrounding young roots. Furthermore, roots leaking oxygen had a higher abundance of sulphide-oxidising cable bacteria; which is the first direct observation of these bacteria on seagrass roots. Thus, ROL may enhance both abiotic and bacterial sulphide oxidation and restrict bacterial sulphide production around vulnerable roots, thereby helping seagrasses to colonise sulphide-rich anoxic sediments.</description><subject>14/19</subject><subject>14/32</subject><subject>14/34</subject><subject>14/63</subject><subject>38/23</subject><subject>38/77</subject><subject>631/326/171</subject><subject>631/449/2668</subject><subject>Abundance</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Biodiversity</subject><subject>Biomedical and Life Sciences</subject><subject>Ecology</subject><subject>Evolutionary Biology</subject><subject>Fluorescence</subject><subject>Geologic Sediments - chemistry</subject><subject>Grasses</subject><subject>Hybridization</subject><subject>Hydrocharitaceae - microbiology</subject><subject>Hydrocharitaceae - physiology</subject><subject>Imaging techniques</subject><subject>Intrusion</subject><subject>Life Sciences</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microorganisms</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Oxygen</subject><subject>Oxygen - metabolism</subject><subject>Plant Roots - microbiology</subject><subject>Plant Roots - physiology</subject><subject>Protective coatings</subject><subject>Rhizosphere</subject><subject>Roots</subject><subject>Seagrasses</subject><subject>Sediments</subject><subject>Spatial distribution</subject><subject>Stress, Physiological</subject><subject>Sulfate reduction</subject><subject>Sulfate-reducing bacteria</subject><subject>Sulfates</subject><subject>Sulfides</subject><subject>Sulfides - metabolism</subject><subject>Thin films</subject><subject>Tips</subject><subject>Zosteraceae - microbiology</subject><subject>Zosteraceae - physiology</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kc9rFTEQx4NYbK3-AV4k4MXL2mSTTbIXQYq_oNCLnkM2md2Xsi95Zna1Bf94U1771EIPIRnmM9_JzJeQV5y940yYM5Rc9Kph3DRMMNN0T8gJ1x1vtNDs6eGt2mPyHPGKsU4rpZ-RY8FEV485Ib8vr28mSHTOiHQseUsR3FRcjUrOC1KfY_IxANJfcdnUcM4poltiTjSPFNd5t6npJl_HEDGmiXo3zEAH5xco0VGXAi0QVl8l7mmKSwHEF-RodDPCy7v7lHz_9PHb-Zfm4vLz1_MPF42Xmi2N74PQUrZsFBA603rZa9GDG1rhuWu9clKpUQgvhWFCwaiC113PQztIEEMvTsn7ve5uHbYQPKSluNnuSty6cmOzi_b_TIobO-WfVklVd2iqwNs7gZJ_rICL3Ub0MM8uQV7Rtryt-zRG84q-eYBe5bWkOl6ljFC674SqFN9TvtTFFxgPn-HM3npr997a6q299dZ2teb1v1McKu7NrEC7B7Cm0gTlb-vHVf8AcCKyYg</recordid><startdate>20190301</startdate><enddate>20190301</enddate><creator>Martin, Belinda C.</creator><creator>Bougoure, Jeremy</creator><creator>Ryan, Megan H.</creator><creator>Bennett, William W.</creator><creator>Colmer, Timothy D.</creator><creator>Joyce, Natalie K.</creator><creator>Olsen, Ylva S.</creator><creator>Kendrick, Gary A.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20190301</creationdate><title>Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress</title><author>Martin, Belinda C. ; Bougoure, Jeremy ; Ryan, Megan H. ; Bennett, William W. ; Colmer, Timothy D. ; Joyce, Natalie K. ; Olsen, Ylva S. ; Kendrick, Gary A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-c9d374420f3ed582c49739eab23c1a2c6a466f33c438036ef6dc7591d2b4e3b93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>14/19</topic><topic>14/32</topic><topic>14/34</topic><topic>14/63</topic><topic>38/23</topic><topic>38/77</topic><topic>631/326/171</topic><topic>631/449/2668</topic><topic>Abundance</topic><topic>Bacteria</topic><topic>Bacteria - 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metabolism</topic><topic>Thin films</topic><topic>Tips</topic><topic>Zosteraceae - microbiology</topic><topic>Zosteraceae - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martin, Belinda C.</creatorcontrib><creatorcontrib>Bougoure, Jeremy</creatorcontrib><creatorcontrib>Ryan, Megan H.</creatorcontrib><creatorcontrib>Bennett, William W.</creatorcontrib><creatorcontrib>Colmer, Timothy D.</creatorcontrib><creatorcontrib>Joyce, Natalie K.</creatorcontrib><creatorcontrib>Olsen, Ylva S.</creatorcontrib><creatorcontrib>Kendrick, Gary A.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science 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>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Martin, Belinda C.</au><au>Bougoure, Jeremy</au><au>Ryan, Megan H.</au><au>Bennett, William W.</au><au>Colmer, Timothy D.</au><au>Joyce, Natalie K.</au><au>Olsen, Ylva S.</au><au>Kendrick, Gary A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2019-03-01</date><risdate>2019</risdate><volume>13</volume><issue>3</issue><spage>707</spage><epage>719</epage><pages>707-719</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Seagrasses thrive in anoxic sediments where sulphide can accumulate to phytotoxic levels. So how do seagrasses persist in this environment? Here, we propose that radial oxygen loss (ROL) from actively growing root tips protects seagrasses from sulphide intrusion not only by abiotically oxidising sulphides in the rhizosphere of young roots, but also by influencing the abundance and spatial distribution of sulphate-reducing and sulphide-oxidising bacteria. We used a novel multifaceted approach combining imaging techniques (confocal fluorescence in situ hybridisation, oxygen planar optodes, and sulphide diffusive gradients in thin films) with microbial community profiling to build a complete picture of the microenvironment of growing roots of the seagrasses
Halophila ovalis
and
Zostera muelleri
. ROL was restricted to young root tips, indicating that seagrasses will have limited ability to influence sulphide oxidation in bulk sediments. On the microscale, however, ROL corresponded with decreased abundance of potential sulphate-reducing bacteria and decreased sulphide concentrations in the rhizosphere surrounding young roots. Furthermore, roots leaking oxygen had a higher abundance of sulphide-oxidising cable bacteria; which is the first direct observation of these bacteria on seagrass roots. Thus, ROL may enhance both abiotic and bacterial sulphide oxidation and restrict bacterial sulphide production around vulnerable roots, thereby helping seagrasses to colonise sulphide-rich anoxic sediments.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30353038</pmid><doi>10.1038/s41396-018-0308-5</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 14/19 14/32 14/34 14/63 38/23 38/77 631/326/171 631/449/2668 Abundance Bacteria Bacteria - classification Bacteria - genetics Bacteria - metabolism Biodiversity Biomedical and Life Sciences Ecology Evolutionary Biology Fluorescence Geologic Sediments - chemistry Grasses Hybridization Hydrocharitaceae - microbiology Hydrocharitaceae - physiology Imaging techniques Intrusion Life Sciences Microbial Ecology Microbial Genetics and Genomics Microbiology Microorganisms Oxidation Oxidation-Reduction Oxygen Oxygen - metabolism Plant Roots - microbiology Plant Roots - physiology Protective coatings Rhizosphere Roots Seagrasses Sediments Spatial distribution Stress, Physiological Sulfate reduction Sulfate-reducing bacteria Sulfates Sulfides Sulfides - metabolism Thin films Tips Zosteraceae - microbiology Zosteraceae - physiology |
title | Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress |
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