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Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics

Sebastiana Roccuzzo, Narciso Couto, Esther Karunakaran, Rahul Kapoore Orcid Logo, Thomas O. Butler, Joy Mukherjee, Erika M. Hansson, Andrew P. Beckerman, Jagroop Pandhal

Frontiers in Microbiology, Volume: 11

Swansea University Author: Rahul Kapoore Orcid Logo

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Abstract

Microalgae can respond to natural cues from crustacean grazers, such as Daphnia, by forming colonies and aggregations called flocs. Combining microalgal biology, physiological ecology, and quantitative proteomics, we identified how infochemicals from Daphnia trigger physiological and cellular level...

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Published in: Frontiers in Microbiology
ISSN: 1664-302X
Published: Frontiers Media SA 2020
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Combining microalgal biology, physiological ecology, and quantitative proteomics, we identified how infochemicals from Daphnia trigger physiological and cellular level changes in the microalga Scenedesmus subspicatus, underpinning colony formation and flocculation. We discovered that flocculation occurs at an energy-demanding &#x2018;alarm&#x2019; phase, with an important role proposed in cysteine synthesis. Flocculation appeared to be initially stimulated by the production of an extracellular matrix where polysaccharides and fatty acids were present, and later sustained at an &#x2018;acclimation&#x2019; stage through mitogen-activated protein kinase (MAPK) signaling cascades. Colony formation required investment into fatty acid metabolism, likely linked to separation of membranes during cell division. Higher energy demands were required at the alarm phase, which subsequently decreased at the acclimation stage, thus suggesting a trade-off between colony formation and flocculation. 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spelling 2021-09-20T14:47:14.6320068 v2 57711 2021-08-30 Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics 5583be4600daecd670edac16f6e77e88 0000-0002-2287-0619 Rahul Kapoore Rahul Kapoore true false 2021-08-30 SBI Microalgae can respond to natural cues from crustacean grazers, such as Daphnia, by forming colonies and aggregations called flocs. Combining microalgal biology, physiological ecology, and quantitative proteomics, we identified how infochemicals from Daphnia trigger physiological and cellular level changes in the microalga Scenedesmus subspicatus, underpinning colony formation and flocculation. We discovered that flocculation occurs at an energy-demanding ‘alarm’ phase, with an important role proposed in cysteine synthesis. Flocculation appeared to be initially stimulated by the production of an extracellular matrix where polysaccharides and fatty acids were present, and later sustained at an ‘acclimation’ stage through mitogen-activated protein kinase (MAPK) signaling cascades. Colony formation required investment into fatty acid metabolism, likely linked to separation of membranes during cell division. Higher energy demands were required at the alarm phase, which subsequently decreased at the acclimation stage, thus suggesting a trade-off between colony formation and flocculation. From an ecological and evolutionary perspective, our findings represent an improved understanding of the effect of infochemicals on microalgae-grazers interactions, and how they can therefore potentially impact on the structure of aquatic communities. Moreover, the mechanisms revealed are of interest in algal biotechnology, for exploitation in low-cost, sustainable microalgal biomass harvesting. Journal Article Frontiers in Microbiology 11 Frontiers Media SA 1664-302X Daphnia infochemicals, Scenedesmus, induced defenses, flocculation, colony formation,physiological ecology, iTRAQ proteomics 7 5 2020 2020-05-07 10.3389/fmicb.2020.00792 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University The work in this manuscript was supported by funding from the Research of the Future 2022, Biohybrid Network Scholarship (The University of Sheffield) and a PHYCONET (BBSRC Network in Industrial Biotechnology and Bioenergy (NIBB) Business Interaction Voucher (BBSRC BB/L013789/1). BB/L013789/1 2021-09-20T14:47:14.6320068 2021-08-30T14:57:09.8631325 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Sebastiana Roccuzzo 1 Narciso Couto 2 Esther Karunakaran 3 Rahul Kapoore 0000-0002-2287-0619 4 Thomas O. Butler 5 Joy Mukherjee 6 Erika M. Hansson 7 Andrew P. Beckerman 8 Jagroop Pandhal 9 57711__20719__7d864e743fcb43dcb3c60ad4cc520474.pdf 57711.VOR.fmicb-11-00792.pdf 2021-08-30T15:00:57.2333828 Output 3115675 application/pdf Version of Record true Copyright: The Authors. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. true eng http://creativecommons.org/licenses/by/4.0/
title Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
spellingShingle Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
Rahul Kapoore
title_short Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
title_full Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
title_fullStr Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
title_full_unstemmed Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
title_sort Metabolic Insights Into Infochemicals Induced Colony Formation and Flocculation in Scenedesmus subspicatus Unraveled by Quantitative Proteomics
author_id_str_mv 5583be4600daecd670edac16f6e77e88
author_id_fullname_str_mv 5583be4600daecd670edac16f6e77e88_***_Rahul Kapoore
author Rahul Kapoore
author2 Sebastiana Roccuzzo
Narciso Couto
Esther Karunakaran
Rahul Kapoore
Thomas O. Butler
Joy Mukherjee
Erika M. Hansson
Andrew P. Beckerman
Jagroop Pandhal
format Journal article
container_title Frontiers in Microbiology
container_volume 11
publishDate 2020
institution Swansea University
issn 1664-302X
doi_str_mv 10.3389/fmicb.2020.00792
publisher Frontiers Media SA
college_str Faculty of Science and Engineering
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hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
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description Microalgae can respond to natural cues from crustacean grazers, such as Daphnia, by forming colonies and aggregations called flocs. Combining microalgal biology, physiological ecology, and quantitative proteomics, we identified how infochemicals from Daphnia trigger physiological and cellular level changes in the microalga Scenedesmus subspicatus, underpinning colony formation and flocculation. We discovered that flocculation occurs at an energy-demanding ‘alarm’ phase, with an important role proposed in cysteine synthesis. Flocculation appeared to be initially stimulated by the production of an extracellular matrix where polysaccharides and fatty acids were present, and later sustained at an ‘acclimation’ stage through mitogen-activated protein kinase (MAPK) signaling cascades. Colony formation required investment into fatty acid metabolism, likely linked to separation of membranes during cell division. Higher energy demands were required at the alarm phase, which subsequently decreased at the acclimation stage, thus suggesting a trade-off between colony formation and flocculation. From an ecological and evolutionary perspective, our findings represent an improved understanding of the effect of infochemicals on microalgae-grazers interactions, and how they can therefore potentially impact on the structure of aquatic communities. Moreover, the mechanisms revealed are of interest in algal biotechnology, for exploitation in low-cost, sustainable microalgal biomass harvesting.
published_date 2020-05-07T04:13:39Z
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