Aquaculture production of hatchling Hawaiian Bobtail Squid (Euprymna scolopes) is negatively impacted by decreasing environmental microbiome diversity
Aims The Hawaiian Bobtail Squid (Euprymna scolopes) is a model organism for investigating host–symbiont relationships. The current scientific focus is on the microbiome within E. scolopes, while very little is known about the microbiome of the tanks housing E. scolopes. We examined the hypothesis th...
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| Veröffentlicht in: | Journal of applied microbiology 2022-03, Vol.132 (3), p.1724-1737 |
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| creator | Murphy, Trevor R. Xiao, Rui Brooks, Marjorie L. Rader, Bethany A. Hamilton‐Brehm, Scott D. |
| description | Aims
The Hawaiian Bobtail Squid (Euprymna scolopes) is a model organism for investigating host–symbiont relationships. The current scientific focus is on the microbiome within E. scolopes, while very little is known about the microbiome of the tanks housing E. scolopes. We examined the hypothesis that bacterial communities and geochemistry within the squid tank environment correlate with the production of viable paralarval squid.
Methods and Results
Total DNA was extracted from sediment and filtered water samples from ‘productive’ squid cohorts with high embryonic survival and paralarval hatching, ‘unproductive’ cohorts with low embryonic survival and paralarval hatching. As a control total DNA was extracted from environmental marine locations where E. scolopes is indigenous. Comparative analysis of the bacterial communities by the 16S rRNA gene was performed using next generation sequencing. Thirty‐eight differentially abundant genera were identified in the adult tank waters. The majority of the sequences represented unclassified, candidate or novel genera. The characterized genera included Aquicella, Woeseia and Ferruginibacter, with Hyphomicrobium and Rhizohapis were found to be more abundant in productive adult tank water. In addition, nitrate and pH covaried with productive cohorts, explaining 67% of the bacterial populations. The lower abundance of nitrate‐reducing bacteria in unproductive adult tank water could explain detected elevated nitrate levels.
Conclusions
We conclude that microbiome composition and water geochemistry can negatively affect E. scolopes reproductive physiology in closed tank systems, ultimately impacting host‐microbe research using these animals.
Significance and Impact of study
These results identify the tight relationship between the microbiome and geochemistry to E. scolopes. From this study, it may be possible to design probiotic counter‐measures to improve aquaculture conditions for E. scolopes. |
| doi_str_mv | 10.1111/jam.15350 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9299211</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2592317373</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4430-ce715e0266713111884b07aea52106fce6f1c5d017304d36c6f819954b5c7983</originalsourceid><addsrcrecordid>eNp1kU9vFCEchidGY2v14BcwJF7aw7T8GZiZi8naVKup8WDvhGF-s8uGgVkYtpkv4ueVdmujJnKBhIeHF96ieEvwOcnjYqvGc8IZx8-KY8IEL6mo6fOHdVVyXNOj4lWMW4wJw1y8LI5YVdOKYXZc_FztktLJzikAmoLvk56Nd8gPaKNmvbHGrdG1ulPGKIc--m5WxqIfu2R6dHqVprCMTqGovfUTxDNkInKwVrPZg12QGSelZ-hRt6AedAAV733g9iZ4N4KblUWj0cF3xo-A-nwsRDMvr4sXg7IR3jzOJ8Xtp6vby-vy5vvnL5erm1JXOX-poSYcMBWiJiz_RNNUHa4VKE4JFoMGMRDNe0xqhqueCS2GhrQtrzqu67ZhJ8WHg3ZK3Qi9zoGCsnIKZlRhkV4Z-feOMxu59nvZ0ralhGTB6aMg-F2COMvRRA3WKgc-RUl5S1m-vWYZff8PuvUpuPw6SQXDTdXWRGTq7EDlP4kxwPAUhmB5X7bMZcuHsjP77s_0T-TvdjNwcQDujIXl_yb5dfXtoPwF5Ri2rg</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2630849716</pqid></control><display><type>article</type><title>Aquaculture production of hatchling Hawaiian Bobtail Squid (Euprymna scolopes) is negatively impacted by decreasing environmental microbiome diversity</title><source>Oxford University Press Journals All Titles (1996-Current)</source><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><creator>Murphy, Trevor R. ; Xiao, Rui ; Brooks, Marjorie L. ; Rader, Bethany A. ; Hamilton‐Brehm, Scott D.</creator><creatorcontrib>Murphy, Trevor R. ; Xiao, Rui ; Brooks, Marjorie L. ; Rader, Bethany A. ; Hamilton‐Brehm, Scott D.</creatorcontrib><description>Aims
The Hawaiian Bobtail Squid (Euprymna scolopes) is a model organism for investigating host–symbiont relationships. The current scientific focus is on the microbiome within E. scolopes, while very little is known about the microbiome of the tanks housing E. scolopes. We examined the hypothesis that bacterial communities and geochemistry within the squid tank environment correlate with the production of viable paralarval squid.
Methods and Results
Total DNA was extracted from sediment and filtered water samples from ‘productive’ squid cohorts with high embryonic survival and paralarval hatching, ‘unproductive’ cohorts with low embryonic survival and paralarval hatching. As a control total DNA was extracted from environmental marine locations where E. scolopes is indigenous. Comparative analysis of the bacterial communities by the 16S rRNA gene was performed using next generation sequencing. Thirty‐eight differentially abundant genera were identified in the adult tank waters. The majority of the sequences represented unclassified, candidate or novel genera. The characterized genera included Aquicella, Woeseia and Ferruginibacter, with Hyphomicrobium and Rhizohapis were found to be more abundant in productive adult tank water. In addition, nitrate and pH covaried with productive cohorts, explaining 67% of the bacterial populations. The lower abundance of nitrate‐reducing bacteria in unproductive adult tank water could explain detected elevated nitrate levels.
Conclusions
We conclude that microbiome composition and water geochemistry can negatively affect E. scolopes reproductive physiology in closed tank systems, ultimately impacting host‐microbe research using these animals.
Significance and Impact of study
These results identify the tight relationship between the microbiome and geochemistry to E. scolopes. From this study, it may be possible to design probiotic counter‐measures to improve aquaculture conditions for E. scolopes.</description><identifier>ISSN: 1364-5072</identifier><identifier>EISSN: 1365-2672</identifier><identifier>DOI: 10.1111/jam.15350</identifier><identifier>PMID: 34724303</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Aliivibrio fischeri - genetics ; Animals ; Aquaculture ; Bacteria ; biodiversity ; Bobtail squid ; Comparative analysis ; Decapodiformes - genetics ; Decapodiformes - microbiology ; Deoxyribonucleic acid ; DNA ; Embryos ; environmental microbiology ; Euprymna scolopes ; Geochemistry ; Hatching ; Hawaii ; Microbiomes ; Microbiota ; Next-generation sequencing ; Nitrates ; Original ; Probiotics ; RNA, Ribosomal, 16S - genetics ; rRNA 16S ; Squid ; Survival ; Symbiosis ; Water analysis ; Water purification ; Water sampling</subject><ispartof>Journal of applied microbiology, 2022-03, Vol.132 (3), p.1724-1737</ispartof><rights>2021 The Authors. published by John Wiley & Sons Ltd on behalf of Society for Applied Microbiology</rights><rights>2021 The Authors. Journal of Applied Microbiology published by John Wiley & Sons Ltd on behalf of Society for Applied Microbiology.</rights><rights>2021. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (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-c4430-ce715e0266713111884b07aea52106fce6f1c5d017304d36c6f819954b5c7983</citedby><cites>FETCH-LOGICAL-c4430-ce715e0266713111884b07aea52106fce6f1c5d017304d36c6f819954b5c7983</cites><orcidid>0000-0003-4178-3497 ; 0000-0002-7474-207X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjam.15350$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjam.15350$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34724303$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Murphy, Trevor R.</creatorcontrib><creatorcontrib>Xiao, Rui</creatorcontrib><creatorcontrib>Brooks, Marjorie L.</creatorcontrib><creatorcontrib>Rader, Bethany A.</creatorcontrib><creatorcontrib>Hamilton‐Brehm, Scott D.</creatorcontrib><title>Aquaculture production of hatchling Hawaiian Bobtail Squid (Euprymna scolopes) is negatively impacted by decreasing environmental microbiome diversity</title><title>Journal of applied microbiology</title><addtitle>J Appl Microbiol</addtitle><description>Aims
The Hawaiian Bobtail Squid (Euprymna scolopes) is a model organism for investigating host–symbiont relationships. The current scientific focus is on the microbiome within E. scolopes, while very little is known about the microbiome of the tanks housing E. scolopes. We examined the hypothesis that bacterial communities and geochemistry within the squid tank environment correlate with the production of viable paralarval squid.
Methods and Results
Total DNA was extracted from sediment and filtered water samples from ‘productive’ squid cohorts with high embryonic survival and paralarval hatching, ‘unproductive’ cohorts with low embryonic survival and paralarval hatching. As a control total DNA was extracted from environmental marine locations where E. scolopes is indigenous. Comparative analysis of the bacterial communities by the 16S rRNA gene was performed using next generation sequencing. Thirty‐eight differentially abundant genera were identified in the adult tank waters. The majority of the sequences represented unclassified, candidate or novel genera. The characterized genera included Aquicella, Woeseia and Ferruginibacter, with Hyphomicrobium and Rhizohapis were found to be more abundant in productive adult tank water. In addition, nitrate and pH covaried with productive cohorts, explaining 67% of the bacterial populations. The lower abundance of nitrate‐reducing bacteria in unproductive adult tank water could explain detected elevated nitrate levels.
Conclusions
We conclude that microbiome composition and water geochemistry can negatively affect E. scolopes reproductive physiology in closed tank systems, ultimately impacting host‐microbe research using these animals.
Significance and Impact of study
These results identify the tight relationship between the microbiome and geochemistry to E. scolopes. From this study, it may be possible to design probiotic counter‐measures to improve aquaculture conditions for E. scolopes.</description><subject>Aliivibrio fischeri - genetics</subject><subject>Animals</subject><subject>Aquaculture</subject><subject>Bacteria</subject><subject>biodiversity</subject><subject>Bobtail squid</subject><subject>Comparative analysis</subject><subject>Decapodiformes - genetics</subject><subject>Decapodiformes - microbiology</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Embryos</subject><subject>environmental microbiology</subject><subject>Euprymna scolopes</subject><subject>Geochemistry</subject><subject>Hatching</subject><subject>Hawaii</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Next-generation sequencing</subject><subject>Nitrates</subject><subject>Original</subject><subject>Probiotics</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>rRNA 16S</subject><subject>Squid</subject><subject>Survival</subject><subject>Symbiosis</subject><subject>Water analysis</subject><subject>Water purification</subject><subject>Water sampling</subject><issn>1364-5072</issn><issn>1365-2672</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kU9vFCEchidGY2v14BcwJF7aw7T8GZiZi8naVKup8WDvhGF-s8uGgVkYtpkv4ueVdmujJnKBhIeHF96ieEvwOcnjYqvGc8IZx8-KY8IEL6mo6fOHdVVyXNOj4lWMW4wJw1y8LI5YVdOKYXZc_FztktLJzikAmoLvk56Nd8gPaKNmvbHGrdG1ulPGKIc--m5WxqIfu2R6dHqVprCMTqGovfUTxDNkInKwVrPZg12QGSelZ-hRt6AedAAV733g9iZ4N4KblUWj0cF3xo-A-nwsRDMvr4sXg7IR3jzOJ8Xtp6vby-vy5vvnL5erm1JXOX-poSYcMBWiJiz_RNNUHa4VKE4JFoMGMRDNe0xqhqueCS2GhrQtrzqu67ZhJ8WHg3ZK3Qi9zoGCsnIKZlRhkV4Z-feOMxu59nvZ0ralhGTB6aMg-F2COMvRRA3WKgc-RUl5S1m-vWYZff8PuvUpuPw6SQXDTdXWRGTq7EDlP4kxwPAUhmB5X7bMZcuHsjP77s_0T-TvdjNwcQDujIXl_yb5dfXtoPwF5Ri2rg</recordid><startdate>202203</startdate><enddate>202203</enddate><creator>Murphy, Trevor R.</creator><creator>Xiao, Rui</creator><creator>Brooks, Marjorie L.</creator><creator>Rader, Bethany A.</creator><creator>Hamilton‐Brehm, Scott D.</creator><general>Oxford University Press</general><general>John Wiley and Sons Inc</general><scope>24P</scope><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>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7TM</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4178-3497</orcidid><orcidid>https://orcid.org/0000-0002-7474-207X</orcidid></search><sort><creationdate>202203</creationdate><title>Aquaculture production of hatchling Hawaiian Bobtail Squid (Euprymna scolopes) is negatively impacted by decreasing environmental microbiome diversity</title><author>Murphy, Trevor R. ; Xiao, Rui ; Brooks, Marjorie L. ; Rader, Bethany A. ; Hamilton‐Brehm, Scott D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4430-ce715e0266713111884b07aea52106fce6f1c5d017304d36c6f819954b5c7983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aliivibrio fischeri - genetics</topic><topic>Animals</topic><topic>Aquaculture</topic><topic>Bacteria</topic><topic>biodiversity</topic><topic>Bobtail squid</topic><topic>Comparative analysis</topic><topic>Decapodiformes - genetics</topic><topic>Decapodiformes - microbiology</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Embryos</topic><topic>environmental microbiology</topic><topic>Euprymna scolopes</topic><topic>Geochemistry</topic><topic>Hatching</topic><topic>Hawaii</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Next-generation sequencing</topic><topic>Nitrates</topic><topic>Original</topic><topic>Probiotics</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>rRNA 16S</topic><topic>Squid</topic><topic>Survival</topic><topic>Symbiosis</topic><topic>Water analysis</topic><topic>Water purification</topic><topic>Water sampling</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Murphy, Trevor R.</creatorcontrib><creatorcontrib>Xiao, Rui</creatorcontrib><creatorcontrib>Brooks, Marjorie L.</creatorcontrib><creatorcontrib>Rader, Bethany A.</creatorcontrib><creatorcontrib>Hamilton‐Brehm, Scott D.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of applied microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Murphy, Trevor R.</au><au>Xiao, Rui</au><au>Brooks, Marjorie L.</au><au>Rader, Bethany A.</au><au>Hamilton‐Brehm, Scott D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Aquaculture production of hatchling Hawaiian Bobtail Squid (Euprymna scolopes) is negatively impacted by decreasing environmental microbiome diversity</atitle><jtitle>Journal of applied microbiology</jtitle><addtitle>J Appl Microbiol</addtitle><date>2022-03</date><risdate>2022</risdate><volume>132</volume><issue>3</issue><spage>1724</spage><epage>1737</epage><pages>1724-1737</pages><issn>1364-5072</issn><eissn>1365-2672</eissn><abstract>Aims
The Hawaiian Bobtail Squid (Euprymna scolopes) is a model organism for investigating host–symbiont relationships. The current scientific focus is on the microbiome within E. scolopes, while very little is known about the microbiome of the tanks housing E. scolopes. We examined the hypothesis that bacterial communities and geochemistry within the squid tank environment correlate with the production of viable paralarval squid.
Methods and Results
Total DNA was extracted from sediment and filtered water samples from ‘productive’ squid cohorts with high embryonic survival and paralarval hatching, ‘unproductive’ cohorts with low embryonic survival and paralarval hatching. As a control total DNA was extracted from environmental marine locations where E. scolopes is indigenous. Comparative analysis of the bacterial communities by the 16S rRNA gene was performed using next generation sequencing. Thirty‐eight differentially abundant genera were identified in the adult tank waters. The majority of the sequences represented unclassified, candidate or novel genera. The characterized genera included Aquicella, Woeseia and Ferruginibacter, with Hyphomicrobium and Rhizohapis were found to be more abundant in productive adult tank water. In addition, nitrate and pH covaried with productive cohorts, explaining 67% of the bacterial populations. The lower abundance of nitrate‐reducing bacteria in unproductive adult tank water could explain detected elevated nitrate levels.
Conclusions
We conclude that microbiome composition and water geochemistry can negatively affect E. scolopes reproductive physiology in closed tank systems, ultimately impacting host‐microbe research using these animals.
Significance and Impact of study
These results identify the tight relationship between the microbiome and geochemistry to E. scolopes. From this study, it may be possible to design probiotic counter‐measures to improve aquaculture conditions for E. scolopes.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>34724303</pmid><doi>10.1111/jam.15350</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-4178-3497</orcidid><orcidid>https://orcid.org/0000-0002-7474-207X</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Aliivibrio fischeri - genetics Animals Aquaculture Bacteria biodiversity Bobtail squid Comparative analysis Decapodiformes - genetics Decapodiformes - microbiology Deoxyribonucleic acid DNA Embryos environmental microbiology Euprymna scolopes Geochemistry Hatching Hawaii Microbiomes Microbiota Next-generation sequencing Nitrates Original Probiotics RNA, Ribosomal, 16S - genetics rRNA 16S Squid Survival Symbiosis Water analysis Water purification Water sampling |
| title | Aquaculture production of hatchling Hawaiian Bobtail Squid (Euprymna scolopes) is negatively impacted by decreasing environmental microbiome diversity |
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