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Irreversible collective migration of cyanobacteria in eutrophic conditions
In response to natural or anthropocentric pollutions coupled to global climate changes, microorganisms from aquatic environments can suddenly accumulate on water surface. These dense suspensions, known as blooms, are harmful to ecosystems and significantly degrade the quality of water resources. In...
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Published in: | PloS one 2015-03, Vol.10 (3), p.e0120906-e0120906 |
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description | In response to natural or anthropocentric pollutions coupled to global climate changes, microorganisms from aquatic environments can suddenly accumulate on water surface. These dense suspensions, known as blooms, are harmful to ecosystems and significantly degrade the quality of water resources. In order to determine the physico-chemical parameters involved in their formation and quantitatively predict their appearance, we successfully reproduced irreversible cyanobacterial blooms in vitro. By combining chemical, biochemical and hydrodynamic evidences, we identify a mechanism, unrelated to the presence of internal gas vesicles, allowing the sudden collective upward migration in test tubes of several cyanobacterial strains (Microcystis aeruginosa PCC 7005, Microcystis aeruginosa PCC 7806 and Synechocystis sp. PCC 6803). The final state consists in a foamy layer of biomass at the air-liquid interface, in which micro-organisms remain alive for weeks, the medium lying below being almost completely depleted of cyanobacteria. These "laboratory blooms" start with the aggregation of cells at high ionic force in cyanobacterial strains that produce anionic extracellular polymeric substances (EPS). Under appropriate conditions of nutrients and light intensity, the high photosynthetic activity within cell clusters leads the dissolved oxygen (DO) to supersaturate and to nucleate into bubbles. Trapped within the EPS, these bubbles grow until their buoyancy pulls the biomass towards the free surface. By investigating a wide range of spatially homogeneous environmental conditions (illumination, salinity, cell and nutrient concentration) we identify species-dependent thresholds and timescales for bloom formation. We conclude on the relevance of such results for cyanobacterial bloom formation in the environment and we propose an efficient method for biomass harvesting in bioreactors. |
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These dense suspensions, known as blooms, are harmful to ecosystems and significantly degrade the quality of water resources. In order to determine the physico-chemical parameters involved in their formation and quantitatively predict their appearance, we successfully reproduced irreversible cyanobacterial blooms in vitro. By combining chemical, biochemical and hydrodynamic evidences, we identify a mechanism, unrelated to the presence of internal gas vesicles, allowing the sudden collective upward migration in test tubes of several cyanobacterial strains (Microcystis aeruginosa PCC 7005, Microcystis aeruginosa PCC 7806 and Synechocystis sp. PCC 6803). The final state consists in a foamy layer of biomass at the air-liquid interface, in which micro-organisms remain alive for weeks, the medium lying below being almost completely depleted of cyanobacteria. These "laboratory blooms" start with the aggregation of cells at high ionic force in cyanobacterial strains that produce anionic extracellular polymeric substances (EPS). Under appropriate conditions of nutrients and light intensity, the high photosynthetic activity within cell clusters leads the dissolved oxygen (DO) to supersaturate and to nucleate into bubbles. Trapped within the EPS, these bubbles grow until their buoyancy pulls the biomass towards the free surface. By investigating a wide range of spatially homogeneous environmental conditions (illumination, salinity, cell and nutrient concentration) we identify species-dependent thresholds and timescales for bloom formation. We conclude on the relevance of such results for cyanobacterial bloom formation in the environment and we propose an efficient method for biomass harvesting in bioreactors.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0120906</identifier><identifier>PMID: 25799424</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aquatic environment ; Aquatic microorganisms ; Biological Physics ; Biomass ; Bioreactors ; Bubbles ; Carbon ; Cell division ; Climate change ; Condensed Matter ; Cyanobacteria ; Diderot, Denis (1713-1784) ; Dissolved oxygen ; Dose-Response Relationship, Drug ; Dose-Response Relationship, Radiation ; Ecosystems ; Environmental changes ; Environmental conditions ; Eutrophic environments ; Eutrophic waters ; Eutrophication ; Eutrophication - drug effects ; Eutrophication - radiation effects ; Experiments ; Extracellular Space - drug effects ; Extracellular Space - metabolism ; Extracellular Space - radiation effects ; Flocculation ; Fluid Dynamics ; Fluid mechanics ; Free surfaces ; Global climate ; Harvesting ; Hydrodynamics ; Laboratories ; Light ; Light intensity ; Luminous intensity ; Mechanics ; Microcystis ; Microcystis - cytology ; Microcystis - drug effects ; Microcystis - growth & development ; Microcystis - radiation effects ; Microcystis aeruginosa ; Microorganisms ; Movement ; Nonlinear Sciences ; Nutrient concentrations ; Nutrients ; Oxygen ; Oxygen - chemistry ; Pattern Formation and Solitons ; Photosynthesis ; Physics ; Salts - pharmacology ; Soft Condensed Matter ; Strains (organisms) ; Synechocystis ; Synechocystis - cytology ; Synechocystis - drug effects ; Synechocystis - growth & development ; Synechocystis - radiation effects ; Time Factors ; Tubes ; Water quality ; Water resources</subject><ispartof>PloS one, 2015-03, Vol.10 (3), p.e0120906-e0120906</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Dervaux et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2015 Dervaux et al 2015 Dervaux et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-9f2ede842b34f87de3cae938340e6b1c2619623154ae0ab0d4178484d850d4eb3</citedby><cites>FETCH-LOGICAL-c726t-9f2ede842b34f87de3cae938340e6b1c2619623154ae0ab0d4178484d850d4eb3</cites><orcidid>0009-0003-5170-8092 ; 0000-0002-2878-4279 ; 0000-0001-8487-5362</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1667181135/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1667181135?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25799424$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01163358$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Chauvat, Franck</contributor><creatorcontrib>Dervaux, Julien</creatorcontrib><creatorcontrib>Mejean, Annick</creatorcontrib><creatorcontrib>Brunet, Philippe</creatorcontrib><title>Irreversible collective migration of cyanobacteria in eutrophic conditions</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In response to natural or anthropocentric pollutions coupled to global climate changes, microorganisms from aquatic environments can suddenly accumulate on water surface. These dense suspensions, known as blooms, are harmful to ecosystems and significantly degrade the quality of water resources. In order to determine the physico-chemical parameters involved in their formation and quantitatively predict their appearance, we successfully reproduced irreversible cyanobacterial blooms in vitro. By combining chemical, biochemical and hydrodynamic evidences, we identify a mechanism, unrelated to the presence of internal gas vesicles, allowing the sudden collective upward migration in test tubes of several cyanobacterial strains (Microcystis aeruginosa PCC 7005, Microcystis aeruginosa PCC 7806 and Synechocystis sp. PCC 6803). The final state consists in a foamy layer of biomass at the air-liquid interface, in which micro-organisms remain alive for weeks, the medium lying below being almost completely depleted of cyanobacteria. These "laboratory blooms" start with the aggregation of cells at high ionic force in cyanobacterial strains that produce anionic extracellular polymeric substances (EPS). Under appropriate conditions of nutrients and light intensity, the high photosynthetic activity within cell clusters leads the dissolved oxygen (DO) to supersaturate and to nucleate into bubbles. Trapped within the EPS, these bubbles grow until their buoyancy pulls the biomass towards the free surface. By investigating a wide range of spatially homogeneous environmental conditions (illumination, salinity, cell and nutrient concentration) we identify species-dependent thresholds and timescales for bloom formation. We conclude on the relevance of such results for cyanobacterial bloom formation in the environment and we propose an efficient method for biomass harvesting in bioreactors.</description><subject>Aquatic environment</subject><subject>Aquatic microorganisms</subject><subject>Biological Physics</subject><subject>Biomass</subject><subject>Bioreactors</subject><subject>Bubbles</subject><subject>Carbon</subject><subject>Cell division</subject><subject>Climate change</subject><subject>Condensed Matter</subject><subject>Cyanobacteria</subject><subject>Diderot, Denis (1713-1784)</subject><subject>Dissolved oxygen</subject><subject>Dose-Response Relationship, Drug</subject><subject>Dose-Response Relationship, Radiation</subject><subject>Ecosystems</subject><subject>Environmental changes</subject><subject>Environmental conditions</subject><subject>Eutrophic environments</subject><subject>Eutrophic waters</subject><subject>Eutrophication</subject><subject>Eutrophication - drug effects</subject><subject>Eutrophication - radiation effects</subject><subject>Experiments</subject><subject>Extracellular Space - drug effects</subject><subject>Extracellular Space - metabolism</subject><subject>Extracellular Space - radiation effects</subject><subject>Flocculation</subject><subject>Fluid Dynamics</subject><subject>Fluid mechanics</subject><subject>Free surfaces</subject><subject>Global climate</subject><subject>Harvesting</subject><subject>Hydrodynamics</subject><subject>Laboratories</subject><subject>Light</subject><subject>Light intensity</subject><subject>Luminous intensity</subject><subject>Mechanics</subject><subject>Microcystis</subject><subject>Microcystis - cytology</subject><subject>Microcystis - drug effects</subject><subject>Microcystis - growth & development</subject><subject>Microcystis - radiation effects</subject><subject>Microcystis aeruginosa</subject><subject>Microorganisms</subject><subject>Movement</subject><subject>Nonlinear Sciences</subject><subject>Nutrient concentrations</subject><subject>Nutrients</subject><subject>Oxygen</subject><subject>Oxygen - chemistry</subject><subject>Pattern Formation and Solitons</subject><subject>Photosynthesis</subject><subject>Physics</subject><subject>Salts - pharmacology</subject><subject>Soft Condensed Matter</subject><subject>Strains (organisms)</subject><subject>Synechocystis</subject><subject>Synechocystis - cytology</subject><subject>Synechocystis - drug effects</subject><subject>Synechocystis - growth & development</subject><subject>Synechocystis - radiation effects</subject><subject>Time Factors</subject><subject>Tubes</subject><subject>Water quality</subject><subject>Water resources</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11r2zAUhs3YWLtu_2BshsFYL5Lpy5J8MwhlWzMChX3dClk-ThQUK5PssP77KYlb4tKLoQuL4-d9Jb3SybLXGE0xFfjj2veh1W669S1MESaoRPxJdo5LSiacIPr0ZH6WvYhxjVBBJefPszNSiLJkhJ1n3-YhwA5CtJWD3HjnwHR2B_nGLoPurG9z3-TmVre-0qaDYHVu2xz6LvjtypokaWu75-LL7FmjXYRXw_ci-_Xl88-r68ni5uv8araYGEF4NykbAjVIRirKGilqoEZDSSVlCHiFDeG45ITigmlAukI1w0IyyWpZpDlU9CJ7e_TdOh_VEENUmHOBJca0SMT8SNRer9U22I0Ot8prqw4FH5ZKh84aB4rWBAsotKkqyUpWljVGnJWGFaasGYXk9WlYra82UBtou6DdyHT8p7UrtfQ7xahAgpJkcHk0WD2QXc8Wal9DGHNKC7nDif0wLBb8nx5ipzY2GnBOt-D7wxm5IEwKmdB3D9DHkxiopU6HtW3j0x7N3lTNGCFFylXQRE0fodKoYWPTBUNjU30kuBwJEtPB326p-xjV_Mf3_2dvfo_Z9yfsCrTrVtG7_vC-xiA7gib4GAM098lipPbtcZeG2reHGtojyd6cXua96K4f6D_MmQkO</recordid><startdate>20150323</startdate><enddate>20150323</enddate><creator>Dervaux, Julien</creator><creator>Mejean, Annick</creator><creator>Brunet, Philippe</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0009-0003-5170-8092</orcidid><orcidid>https://orcid.org/0000-0002-2878-4279</orcidid><orcidid>https://orcid.org/0000-0001-8487-5362</orcidid></search><sort><creationdate>20150323</creationdate><title>Irreversible collective migration of cyanobacteria in eutrophic conditions</title><author>Dervaux, Julien ; Mejean, Annick ; Brunet, Philippe</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-9f2ede842b34f87de3cae938340e6b1c2619623154ae0ab0d4178484d850d4eb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Aquatic environment</topic><topic>Aquatic microorganisms</topic><topic>Biological Physics</topic><topic>Biomass</topic><topic>Bioreactors</topic><topic>Bubbles</topic><topic>Carbon</topic><topic>Cell division</topic><topic>Climate change</topic><topic>Condensed Matter</topic><topic>Cyanobacteria</topic><topic>Diderot, Denis (1713-1784)</topic><topic>Dissolved oxygen</topic><topic>Dose-Response Relationship, Drug</topic><topic>Dose-Response Relationship, Radiation</topic><topic>Ecosystems</topic><topic>Environmental changes</topic><topic>Environmental conditions</topic><topic>Eutrophic environments</topic><topic>Eutrophic waters</topic><topic>Eutrophication</topic><topic>Eutrophication - drug effects</topic><topic>Eutrophication - radiation effects</topic><topic>Experiments</topic><topic>Extracellular Space - drug effects</topic><topic>Extracellular Space - metabolism</topic><topic>Extracellular Space - radiation effects</topic><topic>Flocculation</topic><topic>Fluid Dynamics</topic><topic>Fluid mechanics</topic><topic>Free surfaces</topic><topic>Global climate</topic><topic>Harvesting</topic><topic>Hydrodynamics</topic><topic>Laboratories</topic><topic>Light</topic><topic>Light intensity</topic><topic>Luminous intensity</topic><topic>Mechanics</topic><topic>Microcystis</topic><topic>Microcystis - cytology</topic><topic>Microcystis - drug effects</topic><topic>Microcystis - growth & development</topic><topic>Microcystis - radiation effects</topic><topic>Microcystis aeruginosa</topic><topic>Microorganisms</topic><topic>Movement</topic><topic>Nonlinear Sciences</topic><topic>Nutrient concentrations</topic><topic>Nutrients</topic><topic>Oxygen</topic><topic>Oxygen - chemistry</topic><topic>Pattern Formation and Solitons</topic><topic>Photosynthesis</topic><topic>Physics</topic><topic>Salts - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dervaux, Julien</au><au>Mejean, Annick</au><au>Brunet, Philippe</au><au>Chauvat, Franck</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Irreversible collective migration of cyanobacteria in eutrophic conditions</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-03-23</date><risdate>2015</risdate><volume>10</volume><issue>3</issue><spage>e0120906</spage><epage>e0120906</epage><pages>e0120906-e0120906</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In response to natural or anthropocentric pollutions coupled to global climate changes, microorganisms from aquatic environments can suddenly accumulate on water surface. These dense suspensions, known as blooms, are harmful to ecosystems and significantly degrade the quality of water resources. In order to determine the physico-chemical parameters involved in their formation and quantitatively predict their appearance, we successfully reproduced irreversible cyanobacterial blooms in vitro. By combining chemical, biochemical and hydrodynamic evidences, we identify a mechanism, unrelated to the presence of internal gas vesicles, allowing the sudden collective upward migration in test tubes of several cyanobacterial strains (Microcystis aeruginosa PCC 7005, Microcystis aeruginosa PCC 7806 and Synechocystis sp. PCC 6803). The final state consists in a foamy layer of biomass at the air-liquid interface, in which micro-organisms remain alive for weeks, the medium lying below being almost completely depleted of cyanobacteria. These "laboratory blooms" start with the aggregation of cells at high ionic force in cyanobacterial strains that produce anionic extracellular polymeric substances (EPS). Under appropriate conditions of nutrients and light intensity, the high photosynthetic activity within cell clusters leads the dissolved oxygen (DO) to supersaturate and to nucleate into bubbles. Trapped within the EPS, these bubbles grow until their buoyancy pulls the biomass towards the free surface. By investigating a wide range of spatially homogeneous environmental conditions (illumination, salinity, cell and nutrient concentration) we identify species-dependent thresholds and timescales for bloom formation. We conclude on the relevance of such results for cyanobacterial bloom formation in the environment and we propose an efficient method for biomass harvesting in bioreactors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25799424</pmid><doi>10.1371/journal.pone.0120906</doi><orcidid>https://orcid.org/0009-0003-5170-8092</orcidid><orcidid>https://orcid.org/0000-0002-2878-4279</orcidid><orcidid>https://orcid.org/0000-0001-8487-5362</orcidid><oa>free_for_read</oa></addata></record> |
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recordid | cdi_plos_journals_1667181135 |
source | PubMed (Medline); Publicly Available Content Database (Proquest) (PQ_SDU_P3) |
subjects | Aquatic environment Aquatic microorganisms Biological Physics Biomass Bioreactors Bubbles Carbon Cell division Climate change Condensed Matter Cyanobacteria Diderot, Denis (1713-1784) Dissolved oxygen Dose-Response Relationship, Drug Dose-Response Relationship, Radiation Ecosystems Environmental changes Environmental conditions Eutrophic environments Eutrophic waters Eutrophication Eutrophication - drug effects Eutrophication - radiation effects Experiments Extracellular Space - drug effects Extracellular Space - metabolism Extracellular Space - radiation effects Flocculation Fluid Dynamics Fluid mechanics Free surfaces Global climate Harvesting Hydrodynamics Laboratories Light Light intensity Luminous intensity Mechanics Microcystis Microcystis - cytology Microcystis - drug effects Microcystis - growth & development Microcystis - radiation effects Microcystis aeruginosa Microorganisms Movement Nonlinear Sciences Nutrient concentrations Nutrients Oxygen Oxygen - chemistry Pattern Formation and Solitons Photosynthesis Physics Salts - pharmacology Soft Condensed Matter Strains (organisms) Synechocystis Synechocystis - cytology Synechocystis - drug effects Synechocystis - growth & development Synechocystis - radiation effects Time Factors Tubes Water quality Water resources |
title | Irreversible collective migration of cyanobacteria in eutrophic conditions |
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