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Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)

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 mutab...

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Autores principales: Alsufyani, Taghreed, Califano, Gianmaria, Deicke, Michael, Grueneberg, Jan, Weiss, Anne, Engelen, Aschwin H, Kwantes, Michiel, Mohr, Jan Frieder, Ulrich, Johann F, Wichard, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7289720/
https://www.ncbi.nlm.nih.gov/pubmed/32016363
http://dx.doi.org/10.1093/jxb/eraa066
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author Alsufyani, Taghreed
Califano, Gianmaria
Deicke, Michael
Grueneberg, Jan
Weiss, Anne
Engelen, Aschwin H
Kwantes, Michiel
Mohr, Jan Frieder
Ulrich, Johann F
Wichard, Thomas
author_facet Alsufyani, Taghreed
Califano, Gianmaria
Deicke, Michael
Grueneberg, Jan
Weiss, Anne
Engelen, Aschwin H
Kwantes, Michiel
Mohr, Jan Frieder
Ulrich, Johann F
Wichard, Thomas
author_sort Alsufyani, Taghreed
collection PubMed
description 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(−1). We demonstrated that gametes acquired the iron complex of thallusin, thereby linking morphogenetic processes with intracellular iron homeostasis. Understanding macroalgae–bacteria interactions permits further elucidation of the evolution of multicellularity and cellular differentiation, and development of new applications in microbiome-mediated aquaculture systems.
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spelling pubmed-72897202020-06-16 Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta) Alsufyani, Taghreed Califano, Gianmaria Deicke, Michael Grueneberg, Jan Weiss, Anne Engelen, Aschwin H Kwantes, Michiel Mohr, Jan Frieder Ulrich, Johann F Wichard, Thomas J Exp Bot Research Papers 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(−1). We demonstrated that gametes acquired the iron complex of thallusin, thereby linking morphogenetic processes with intracellular iron homeostasis. Understanding macroalgae–bacteria interactions permits further elucidation of the evolution of multicellularity and cellular differentiation, and development of new applications in microbiome-mediated aquaculture systems. Oxford University Press 2020-06-11 2020-02-04 /pmc/articles/PMC7289720/ /pubmed/32016363 http://dx.doi.org/10.1093/jxb/eraa066 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Papers
Alsufyani, Taghreed
Califano, Gianmaria
Deicke, Michael
Grueneberg, Jan
Weiss, Anne
Engelen, Aschwin H
Kwantes, Michiel
Mohr, Jan Frieder
Ulrich, Johann F
Wichard, Thomas
Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)
title Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)
title_full Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)
title_fullStr Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)
title_full_unstemmed Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)
title_short Macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta)
title_sort macroalgal–bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed ulva (chlorophyta)
topic Research Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7289720/
https://www.ncbi.nlm.nih.gov/pubmed/32016363
http://dx.doi.org/10.1093/jxb/eraa066
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