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

Abstract

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.

Cultivating the Macroalgal Holobiont: Effects of Integrated Multi-Trophic Aquaculture on the Microbiome of Ulva rigida (Chlorophyta)

“…are of high relevance in macroalgal aquaculture despite their low relative abundances of 0.08, 0.3, and 1.2% in rearing water. Indeed, previous studies highlighted their importance in the morphological development of germlings of U. mutabilis, U. intestinalis, and U. linza (Grueneberg et al, 2016;Ghaderiardakani et al, 2017;Weiss et al, 2017a) through the release of morphogens, such as thallusin, at low concentrations in the fg/ml range, but with high biological activity, that trigger algal growth and morphogenesis (Matsuo et al, 2005;Wichard, 2015;Alsufyani et al, 2020). As we did not test the bioactivity of the bacteria, other unknown taxa adapted to the aquaculture environment might also induce Ulva's morphogenesis.…”

Microbiome-Dependent Adaptation of Seaweeds Under Environmental Stresses: A Perspective

“…The genus is best known for its broad distribution in marine (fully saline), brackish, and freshwater ecosystems in tropical, temperate, and the less-studied polar regions ( Figure 1A). A genetic toolbox was developed, and essential chemical mediators of the algae-bacteria interaction were identified (Joint et al, 2002;Tait et al, 2009;Oertel et al, 2015;De Clerck et al, 2018;Alsufyani et al, 2020).…”

“…Bacteria can be associated with the surface, the holdfast, or the chemical boundary layer of the alga in the surrounding water (Mieszkin et al, 2013;Egan et al, 2014;Wichard, 2015). Based on different scenarios, chemical compounds produced on macroalgal surface or its vicinity may present the primary factors driving the dynamic of bacterial communities within the network of algae-bacteria interactions (Lachnit et al, 2013;Kessler et al, 2018;Alsufyani et al, 2020;Burgunter-Delamare et al, 2020;Paix et al, 2020). Employing a multi-omics approach on the thallus scale demonstrated that chemical production, which is mostly stimulated by the algal physiology, defines the microbial community structure and composition at the surface of individual thalli of Taonia atomaria.…”

“…Within the chemosphere, these organisms interact with each other through chemical mediators such as AGMPFs, nutrients (photosynthates), and bacterial attractants (DMSP) ( Figure 1B). Thallusin has been recently defined as the Maribacter-factor that triggers morphogenesis in U. mutabilis (Alsufyani et al, 2020) and was initially described for the development of Monostroma sp. (Chlorophyta) (Matsuo et al, 2005).…”

“…(Chlorophyta) (Matsuo et al, 2005). Thallusin acts as a morphogen and induces cell differentiation, cell wall development, and rhizoid formation in U. mutabilis at concentrations in the picomole per liter range (Wichard, 2015;Alsufyani et al, 2020). For the release of thallusin and other chemical mediators, both the alga and the associated bacteria that provide those compounds must show an adequate intrinsic stress response.…”