{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,21]],"date-time":"2026-04-21T15:23:31Z","timestamp":1776785011424,"version":"3.51.2"},"reference-count":47,"publisher":"Oxford University Press (OUP)","issue":"11","license":[{"start":{"date-parts":[[2020,2,4]],"date-time":"2020-02-04T00:00:00Z","timestamp":1580774400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["CRC1127"],"award-info":[{"award-number":["CRC1127"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Jena School for Microbial Communication"},{"name":"European Union\u2019s Horizon","award":["642575"],"award-info":[{"award-number":["642575"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,6,11]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Macroalgal microbiomes have core functions related to biofilm formation, growth, and morphogenesis of seaweeds. In particular, the growth and development of the sea lettuce Ulva spp. (Chlorophyta) depend on bacteria releasing morphogenetic compounds. Under axenic conditions, the macroalga Ulva mutabilis develops a callus-like phenotype with cell wall protrusions. However, co-culturing with Roseovarius sp. (MS2) and Maribacter sp. (MS6), which produce various stimulatory chemical mediators, completely recovers morphogenesis. This ecological reconstruction forms a tripartite community which can be further studied for its role in cross-kingdom interactions. Hence, our study sought to identify algal growth- and morphogenesis-promoting factors (AGMPFs) capable of phenocopying the activity of Maribacter spp. We performed bioassay-guided solid-phase extraction in water samples collected from U. mutabilis aquaculture systems. We uncovered novel ecophysiological functions of thallusin, a sesquiterpenoid morphogen, identified for the first time in algal aquaculture. Thallusin, released by Maribacter sp., induced rhizoid and cell wall formation at a concentration of 11 pmol l\u22121. We demonstrated that gametes acquired the iron complex of thallusin, thereby linking morphogenetic processes with intracellular iron homeostasis. Understanding macroalgae\u2013bacteria interactions permits further elucidation of the evolution of multicellularity and cellular differentiation, and development of new applications in microbiome-mediated aquaculture systems.<\/jats:p>","DOI":"10.1093\/jxb\/eraa066","type":"journal-article","created":{"date-parts":[[2020,2,2]],"date-time":"2020-02-02T04:09:05Z","timestamp":1580616545000},"page":"3340-3349","source":"Crossref","is-referenced-by-count":98,"title":["Macroalgal\u2013bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)"],"prefix":"10.1093","volume":"71","author":[{"given":"Taghreed","family":"Alsufyani","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"},{"name":"Algal Research Laboratory, Chemistry Department, Science Faculty, Taif University, Taif, Saudi Arabia"}]},{"given":"Gianmaria","family":"Califano","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"}]},{"given":"Michael","family":"Deicke","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"}]},{"given":"Jan","family":"Grueneberg","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"},{"name":"Jena School for Microbial Communication, Jena, Germany"}]},{"given":"Anne","family":"Weiss","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"},{"name":"Jena School for Microbial Communication, Jena, Germany"}]},{"given":"Aschwin H","family":"Engelen","sequence":"first","affiliation":[{"name":"Centre for Marine Sciences (CCMAR), University of Algarve, Campus de Gambelas, Faro, Portugal"}]},{"given":"Michiel","family":"Kwantes","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"}]},{"given":"Jan Frieder","family":"Mohr","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"},{"name":"Jena School for Microbial Communication, Jena, Germany"}]},{"given":"Johann F","family":"Ulrich","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0061-4160","authenticated-orcid":false,"given":"Thomas","family":"Wichard","sequence":"first","affiliation":[{"name":"Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany"},{"name":"Jena School for Microbial Communication, Jena, Germany"}]}],"member":"286","published-online":{"date-parts":[[2020,2,4]]},"reference":[{"key":"2020061121331822700_CIT0001","doi-asserted-by":"crossref","first-page":"14","DOI":"10.3390\/md15010014","article-title":"Time course exo-metabolomic profiling in the green marine macroalga Ulva (Chlorophyta) for identification of growth phase-dependent biomarkers","volume":"15","author":"Alsufyani","year":"2017","journal-title":"Marine Drugs"},{"key":"2020061121331822700_CIT0002","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1038\/nature14488","article-title":"Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria","volume":"522","author":"Amin","year":"2015","journal-title":"Nature"},{"key":"2020061121331822700_CIT0003","doi-asserted-by":"crossref","first-page":"1756","DOI":"10.3732\/ajb.89.11.1756","article-title":"Novel morphology in Enteromorpha (Ulvophyceae) forming green tides","volume":"89","author":"Blomster","year":"2002","journal-title":"American Journal of Botany"},{"key":"2020061121331822700_CIT0004","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1126\/science.281.5374.207","article-title":"Acquisition and utilization of transition metal ions by marine organisms","volume":"281","author":"Butler","year":"1998","journal-title":"Science"},{"key":"2020061121331822700_CIT0005","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1201\/b21460-9","article-title":"Preparation of axenic cultures in Ulva (Chlorophyta).","volume-title":"Protocols for macroalgae research","author":"Califano","year":"2018"},{"key":"2020061121331822700_CIT0006","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1038\/ncomms1251","article-title":"Trends in the development of environmentally friendly fouling-resistant marine coatings","volume":"2","author":"Callow","year":"2011","journal-title":"Nature Communications"},{"key":"2020061121331822700_CIT0007","first-page":"737","article-title":"Understanding \u2018green\u2019 multicellularity: do seaweeds hold the key?","volume":"5","author":"Coates","year":"2014","journal-title":"Frontiers in Plant Science"},{"key":"2020061121331822700_CIT0008","doi-asserted-by":"crossref","first-page":"2921","DOI":"10.1016\/j.cub.2018.08.015","article-title":"Insights into the evolution of multicellularity from the sea lettuce genome","volume":"28","author":"De Clerck","year":"2018","journal-title":"Current Biology"},{"key":"2020061121331822700_CIT0009","doi-asserted-by":"crossref","first-page":"6096","DOI":"10.1039\/C4AN01461H","article-title":"Metallophore mapping in complex matrices by metal isotope coded profiling of organic ligands","volume":"139","author":"Deicke","year":"2014","journal-title":"The Analyst"},{"key":"2020061121331822700_CIT0010","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1111\/1574-6976.12011","article-title":"The seaweed holobiont: understanding seaweed\u2013bacteria interactions","volume":"37","author":"Egan","year":"2013","journal-title":"FEMS Microbiology Reviews"},{"key":"2020061121331822700_CIT0011","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1007\/978-3-642-61398-2_2","article-title":"The occurrence of green tides\u2014a review.","volume-title":"Marine benthic vegetation","author":"Fletcher","year":"1996"},{"key":"2020061121331822700_CIT0012","first-page":"473","article-title":"\u00dcber die Sexualit\u00e4t und den Generationswechsel von Ulva mutabilis","volume":"102","author":"F\u00f8yn","year":"1958","journal-title":"Archiv f\u00fcr Protistenkunde"},{"key":"2020061121331822700_CIT0046","doi-asserted-by":"crossref","first-page":"2123","DOI":"10.1021\/ol0605777","article-title":"Synthesis of ent-thallusin","volume":"8","author":"Gao","year":"2006","journal-title":"Organic Letters"},{"key":"2020061121331822700_CIT0013","doi-asserted-by":"crossref","first-page":"375","DOI":"10.3354\/aei00319","article-title":"Analysis of algal growth- and morphogenesis-promoting factors in an integrated multi-trophic aquaculture system for farming Ulva spp","volume":"11","author":"Ghaderiardakani","year":"2019","journal-title":"Aquaculture Environment Interactions"},{"key":"2020061121331822700_CIT0014","doi-asserted-by":"crossref","first-page":"fix094","DOI":"10.1093\/femsec\/fix094","article-title":"Bacteria-induced morphogenesis of Ulva intestinalis and Ulva mutabilis (Chlorophyta): a contribution to the lottery theory","volume":"93","author":"Ghaderiardakani","year":"2017","journal-title":"FEMS Microbiology Ecology"},{"key":"2020061121331822700_CIT0015","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1111\/j.0022-3646.1993.00755.x","article-title":"Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation","volume":"29","author":"Geider","year":"1993","journal-title":"Journal of Phycology"},{"key":"2020061121331822700_CIT0016","doi-asserted-by":"crossref","first-page":"267","DOI":"10.3354\/meps08607","article-title":"Chemical interactions between marine macroalgae and bacteria","volume":"409","author":"Goecke","year":"2010","journal-title":"Marine Ecology Progress Series"},{"key":"2020061121331822700_CIT0017","doi-asserted-by":"crossref","first-page":"e0146307","DOI":"10.1371\/journal.pone.0146307","article-title":"Macroalgal morphogenesis induced by waterborne compounds and bacteria in coastal seawater","volume":"11","author":"Grueneberg","year":"2016","journal-title":"PLoS One"},{"key":"2020061121331822700_CIT0018","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1080\/1364253031000136321","article-title":"Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera","volume":"38","author":"Hayden","year":"2003","journal-title":"European Journal of Phycology"},{"key":"2020061121331822700_CIT0019","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1126\/science.1077075","article-title":"Cell-to-cell communication across the prokaryote\u2013eukaryote boundary","volume":"298","author":"Joint","year":"2002","journal-title":"Science"},{"key":"2020061121331822700_CIT0020","doi-asserted-by":"crossref","first-page":"1808","DOI":"10.1111\/mec.14472","article-title":"Macroalgal\u2013bacterial interactions: role of dimethylsulfoniopropionate in microbial gardening by Ulva (Chlorophyta)","volume":"27","author":"Kessler","year":"2018","journal-title":"Molecular Ecology"},{"key":"2020061121331822700_CIT0021","first-page":"77","article-title":"Genetic control of division rate and morphogenesis in Ulva mutabilis F\u00f8yn","volume":"34","author":"L\u00f8vlie","year":"1964","journal-title":"Comptes Rendus des Travaux du Laboratoire Carlsberg"},{"key":"2020061121331822700_CIT0022","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1515\/botm.1978.21.3.155","article-title":"On the relation between sexual and parthenogenetic reproduction in haplo-diplontic algae","volume":"21","author":"L\u00f8vlie","year":"1978","journal-title":"Botanica Marina"},{"key":"2020061121331822700_CIT0023","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1007\/s00248-006-9060-x","article-title":"Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza","volume":"52","author":"Marshall","year":"2006","journal-title":"Microbial Ecology"},{"key":"2020061121331822700_CIT0024","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.1126\/science.1105486","article-title":"Isolation of an algal morphogenesis inducer from a marine bacterium","volume":"307","author":"Matsuo","year":"2005","journal-title":"Science"},{"key":"2020061121331822700_CIT0025","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1046\/j.1462-2920.2003.00382.x","article-title":"Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum","volume":"5","author":"Matsuo","year":"2003","journal-title":"Environmental Microbiology"},{"key":"2020061121331822700_CIT0026","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1111\/j.1365-2958.2009.06932.x","article-title":"Different roles for anti-sigma factors in siderophore signalling pathways of Pseudomonas aeruginosa","volume":"74","author":"Mettrick","year":"2009","journal-title":"Molecular Microbiology"},{"key":"2020061121331822700_CIT0027","doi-asserted-by":"crossref","first-page":"4229","DOI":"10.1016\/j.tetlet.2007.04.075","article-title":"Total synthesis and morphogenesis-inducing activity of (\u00b1)-thallusin and its analogues","volume":"48","author":"Nishizawa","year":"2007","journal-title":"Tetrahedron Letters"},{"key":"2020061121331822700_CIT0028","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1098\/rstb.2011.0252","article-title":"Morphological evolution in land plants: new designs with old genes","volume":"367","author":"Pires","year":"2012","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"key":"2020061121331822700_CIT0029","doi-asserted-by":"crossref","first-page":"375","DOI":"10.2307\/1538992","article-title":"Effect of plant hormones on Ulva","volume":"114","author":"Provasoli","year":"1958","journal-title":"The Biological Bulletin"},{"key":"2020061121331822700_CIT0030","doi-asserted-by":"crossref","first-page":"17065","DOI":"10.1038\/nmicrobiol.2017.65","article-title":"Zooming in on the phycosphere: the ecological interface for phytoplankton\u2013bacteria relationships","volume":"2","author":"Seymour","year":"2017","journal-title":"Nature Microbiology"},{"key":"2020061121331822700_CIT0031","doi-asserted-by":"crossref","first-page":"13","DOI":"10.3354\/ab00312","article-title":"Isolation of seaweed-associated bacteria and their morphogenesis-inducing capability in axenic cultures of the green alga Ulva fasciata","volume":"12","author":"Singh","year":"2011","journal-title":"Aquatic Biology"},{"key":"2020061121331822700_CIT0032","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1038\/nature12860","article-title":"Green and golden seaweed tides on the rise","volume":"504","author":"Smetacek","year":"2013","journal-title":"Nature"},{"key":"2020061121331822700_CIT0033","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1111\/j.1529-8817.2012.01231.x","article-title":"Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors","volume":"48","author":"Spoerner","year":"2012","journal-title":"Journal of Phycology"},{"key":"2020061121331822700_CIT0034","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1111\/jpy.12804","article-title":"Conspecificity of the model organism Ulva mutabilis and Ulva compressa (Ulvophyceae, Chlorophyta)","volume":"55","author":"Steinhagen","year":"2019","journal-title":"Journal of Phycology"},{"key":"2020061121331822700_CIT0035","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1080\/09670262.2018.1513167","article-title":"Molecular analysis of Ulva compressa (Chlorophyta, Ulvales) reveals its morphological plasticity, distribution and potential invasiveness on German North Sea and Baltic Sea coasts","volume":"54","author":"Steinhagen","year":"2019","journal-title":"European Journal of Phycology"},{"key":"2020061121331822700_CIT0036","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1111\/j.0022-3646.1996.01009.x","article-title":"Differentiation of Ulva mutabilis (Chlorophyta) gametangia and gamete release are controlled by extracellular inhibitors","volume":"32","author":"Stratmann","year":"1996","journal-title":"Journal of Phycology"},{"key":"2020061121331822700_CIT0037","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1111\/j.1462-2920.2004.00706.x","article-title":"Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms","volume":"7","author":"Tait","year":"2005","journal-title":"Environmental Microbiology"},{"key":"2020061121331822700_CIT0038","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1093\/oxfordjournals.molbev.a026190","article-title":"Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha","volume":"16","author":"Tan","year":"1999","journal-title":"Molecular Biology and Evolution"},{"key":"2020061121331822700_CIT0039","doi-asserted-by":"crossref","first-page":"15","DOI":"10.3389\/fpls.2015.00015","article-title":"Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): comparison with Ulva mutabilis and potential for laboratory culture","volume":"6","author":"Vesty","year":"2015","journal-title":"Frontiers in Plant Science"},{"key":"2020061121331822700_CIT0040","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1515\/bot-2016-0083","article-title":"Morphogenesis of Ulva mutabilis (Chlorophyta) induced by Maribacter species (Bacteroidetes, Flavobacteriaceae)","volume":"60","author":"Weiss","year":"2017","journal-title":"Botanica Marina"},{"key":"2020061121331822700_CIT0041","doi-asserted-by":"crossref","first-page":"86","DOI":"10.3389\/fpls.2015.00086","article-title":"Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta)","volume":"6","author":"Wichard","year":"2015","journal-title":"Frontiers in Plant Science"},{"key":"2020061121331822700_CIT0047","doi-asserted-by":"crossref","first-page":"131","DOI":"10.3389\/fmars.2016.00131","article-title":"Identification of metallophores and organic ligands in the chemosphere of the marine macroalga Ulva (Chlorophyta) and at land-sea interfaces","volume":"3","author":"Wichard","year":"2016","journal-title":"Frontiers in Marine Science"},{"key":"2020061121331822700_CIT0042","doi-asserted-by":"crossref","first-page":"72","DOI":"10.3389\/fpls.2015.00072","article-title":"The green seaweed Ulva: a model system to study morphogenesis","volume":"6","author":"Wichard","year":"2015","journal-title":"Frontiers in Plant Science"},{"key":"2020061121331822700_CIT0043","doi-asserted-by":"crossref","first-page":"8850","DOI":"10.1021\/jo501720b","article-title":"Total synthesis of (\u2013)-thallusin: utilization of enzymatic hydrolysis resolution","volume":"79","author":"Yamamoto","year":"2014","journal-title":"Journal of Organic Chemistry"},{"key":"2020061121331822700_CIT0044","doi-asserted-by":"crossref","first-page":"7173","DOI":"10.1016\/j.tet.2018.10.048","article-title":"Syntheses of thallusin analogues and their algal morphogenesis-inducing activities","volume":"74","author":"Yamamoto","year":"2018","journal-title":"Tetrahedron"},{"key":"2020061121331822700_CIT0045","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1093\/nsr\/nwz026","article-title":"Ulva prolifera green-tide outbreaks and their environmental impact in the Yellow Sea, China","volume":"6","author":"Zhang","year":"2019","journal-title":"National Science Review"}],"container-title":["Journal of Experimental Botany"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jxb\/advance-article-pdf\/doi\/10.1093\/jxb\/eraa066\/32894482\/eraa066.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jxb\/article-pdf\/71\/11\/3340\/33380216\/eraa066.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jxb\/article-pdf\/71\/11\/3340\/33380216\/eraa066.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,6,12]],"date-time":"2020-06-12T01:33:40Z","timestamp":1591925620000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jxb\/article\/71\/11\/3340\/5721957"}},"subtitle":[],"editor":[{"given":"Andreas","family":"Holzinger","sequence":"first","affiliation":[{"name":"University of Innsbruck, Austria"}]}],"short-title":[],"issued":{"date-parts":[[2020,2,4]]},"references-count":47,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,2,4]]},"published-print":{"date-parts":[[2020,6,11]]}},"URL":"https:\/\/doi.org\/10.1093\/jxb\/eraa066","relation":{},"ISSN":["0022-0957","1460-2431"],"issn-type":[{"value":"0022-0957","type":"print"},{"value":"1460-2431","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,6,11]]},"published":{"date-parts":[[2020,2,4]]}}}