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Morphogenesis of Ulva Mutabilis (Chlorophyta) Induced by Maribacter Species (Bacteroidetes, Flavobacteriaceae)

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Morphogenesis of Ulva Mutabilis (Chlorophyta) Induced by Maribacter Species (Bacteroidetes, Flavobacteriaceae) Botanica Marina 2017; 60(2): 197–206 Short communication Open Access Anne Weiss, Rodrigo Costa and Thomas Wichard* Morphogenesis of Ulva mutabilis (Chlorophyta) induced by Maribacter species (Bacteroidetes, Flavobacteriaceae) DOI 10.1515/bot-2016-0083 related Flavobacteriaceae and a Maribacter strain isolated Received 31 July, 2016; accepted 11 January, 2017; online first from a red alga did not possess any activity. 17 February, 2017 Keywords: bacteroidetes; cell differentiation; green mac- Abstract: Growth and morphogenesis of the sea lettuce Ulva roalga; morphogens; thallusin. (Chlorophyta) depends on the combination of regulative morphogenetic compounds released by specific associated bacteria. Axenic Ulva gametes develop parthenogenetically The green macroalga Ulva mutabilis Føyn (Chlorophyta) is into callus-like colonies consisting of undifferentiated cells not able to develop and differentiate into blade, stem and without normal cell walls. In Ulva mutabilis Føyn, two bac- rhizoid cells under axenic conditions, or when its microbi- terial strains, Maribacter sp. strain MS6 and Roseovarius ome is not appropriate. Instead, the alga forms callus-like, strain MS2, can restore the complete algal morphogenesis slow growing structures with colourless protrusions from forming a tripartite symbiotic community. Morphogenetic the exterior cell wall (Spoerner et al. 2012, Wichard 2015). compounds ( = morphogens) released by the MS6-strain Early experiments of Provasoli (1958) have already pointed induce rhizoid formation and cell wall development in U. out that treatment of Ulva with antibiotics results in abnor- mutabilis, while several bacteria of the Roseobacter clade, mal growth. Further experiments examined the role of including the MS2-strain, promote blade cell division and isolated bacteria in activating developmental and growth thallus elongation. In this study, 12 type strains of the Fla- promoting traits in Ulva and revealed species-specific inter- vobacteriaceae family, including six Maribacter strains, actions, as no combination of bacteria showed the com- were examined for their morphogenetic activity in compari- plete recovery of the normal morphotypes (Provasoli and son to the original MS6-strain isolated from U. mutabilis. Pintner 1980, Marshall et al. 2006, Spoerner et al. 2012, The bioassay is based on the functional complementation Wichard 2015). Two bacterial isolates from non-axenic lab- of the tested Flavobacteriaceae strain with the Roseovarius oratory cultures of U. mutabilis were later found to induce MS2-strain. If the test-strain possesses morphogenetic the complete morphogenesis of U. mutabilis, forming a tri- activity complementary to the factor of the MS2-strain, the partite community (Spoerner et al. 2012, Wichard 2015). The complete morphogenesis of U. mutabilis can be restored. bacterial strains were originally described as Roseobacter This bioassay revealed not only the stand-alone activity of sp. strain MS2 and Cytophaga sp. MS6. The strain MS2 alone certain bacteria, but also their essential capability to take induces cell division and elongation of the blades but not part in the orchestrated bacteria-induced morphogenesis of of the rhizoid, whereas the strain MS6 promotes rhizoid U. mutabilis. All Maribacter type strains isolated from Ulva formation and proper cell wall synthesis without cell-wall could phenocopy the MS6-strain, whereas some distantly protrusions (Figure 1; Spoerner et al. 2012). Overall these morphogenesis-inducing bacteria secreted a bouquet (i.e. MS6- and MS2-factors) of still uncharacterised morpho- *Corresponding author: Thomas Wichard, Institute for Inorganic and Analytical Chemistry, Jena School of Microbial Communication, genesis-inducing factors ( = morphogens) into the culture Friedrich Schiller University Jena, Jena, Lessingstr. 8, 07743 Jena, medium of Ulva (Spoerner et al. 2012). However, each of Germany, e-mail: [email protected] these bacteria can be replaced with partly purified com- Anne Weiss: Institute for Inorganic and Analytical Chemistry, Jena pounds extracted from the corresponding bacterial culture School of Microbial Communication, Friedrich Schiller University medium (Spoerner et al. 2012, Wichard, unpublished Jena, Jena, Lessingstr. 8, 07743 Jena, Germany results). Morphogens with similar activity to the com- Rodrigo Costa: Institute for Bioengineering and Biosciences (IBB), Department of Bioengineering, Instituto Superior Técnico, pounds released by the MS6-strain were also determined in Universidade de Lisboa, Lisbon, Portugal sterile-filtered lagoon water of the Ria Formosa (Portugal) at ©2017, Anne Weiss et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. 198 A. Weiss et al.: Morphogenesis of Ulva Figure 1: Control experiment for complementary activity of morphogenesis-inducing bacteria (reference strains). Axenic Ulva mutabilis sl G mt( + ) germlings (A) were inoculated with either Roseovarius sp. MS2 (B) or Maribacter sp. MS6 (C) or both bacteria (D). Gametophytes were propagated for gamete production and release under laboratory conditions (Wichard and Oertel 2010). Afterwards axenic gametes were prepared according to Wichard (2015). Purified gametes [mating type ( + )] were inoculated with selected bacteria (final concen- − 6 tration OD600 = 1 × 10 ) in 10 ml Ulva culture medium and kept in the dark for 24 h to let gametes settle on culture tissue flask. After 14 days growth at 18°C and 90–120 μmol photons s − 1 m − 2 for 17 h light and 7 h dark, thallus development of 50–70 germlings derived from triplicate experiments was examined with an inverted Leica DMIL LED microscope (Leica, Solms, Germany) equipped with a digital camera (Nikon, Düs- seldorf, Germany). The four morphotypes are colour-coded. Black arrows indicate protrusions from the exterior cell wall. Scale bars = 100 μm. sampling sites where Ulva sp. was usually abundant. These metabolism is aerobic or facultatively anaerobic (Nedashk- results indicated a tight interaction of the MS6-factor-pro- ovskaya et al. 2004a, 2010, Barbeyron et al. 2008, Lo et al. ducing bacterium with Ulva. In contrast, the MS2-like bioac- 2013, Weerawongwiwat et al. 2013, Hu et al. 2015, Jackson tivity factor was abundant all over the lagoon regardless of et al. 2015). They were found in various marine sources and the presence or absence of Ulva species (Grueneberg et al. climatic zones (Cho et al. 2008, Zhang et al. 2009, Tang 2016). In this context further phylogenetic analysis classi- et al. 2015) and could be isolated from the water column fied the MS6-strain to the genus Maribacter rather than to (Yoon et al. 2005, Barbeyron et al. 2008) and the sea sedi- Cytophaga, while the MS2-strain was reclassified to Roseo- ment (Nedashkovskaya et al. 2004a, Cho et al. 2008). varius (Grueneberg et al. 2016). The same study has also Maribacter strains are often associated with the surface shown that cultivable bacteria isolated from the surface of of macroalgae such as Ulva fenestra Postels & Ruprecht Ulva rigida C. Agardh could not replace the eco-physiologi- (Nedashkovskaya et al. 2004a, 2010, Weerawongwiwat cal functions of the Maribacter sp. MS6. The uniqueness of et al. 2013), U. mutabilis (Spoerner et al. 2012) and Polysi- the MS6-factors seems to be produced by difficult-to- culture phonia (Nedashkovskaya et al. 2007), where they harbour bacteria, which may accidentally get lost in the laboratory various enzyme activities involved in degradation of, for (Spoerner et al. 2012, Grueneberg et al. 2016). example, algal polysaccharides (Bakunina et al. 2012). Maribacter is a bacterial genus within the Flavobac- In this study, we tested whether the Maribacter genus, teriaceae comprising 20 documented species at present. and possibly closely related genera, could phenocopy Mar- Maribacter are gram-negative, rod shaped cells, which ibacter sp. MS6 in our tripartite model system (Table 1). produce non-diffusible yellow to orange pigments. The To have morphogenesis-inducing strains available for Table 1: List of Maribacter and other Flavobacteria type- and control-strains selected for bioassay screening on morphogenetic activities on Ulva mutabilis. Name Strain GenBank Source Geographical origin Reference accession # Maribacter sp. (formerly Cytophaga sp.) MS6 EU359911 U. mutabilis Portugal, Ria Formosa Spoerner et al. 2012 Roseovarius sp. (formerly Roseobacter sp.) MS2 EU359909 U. mutabilis Portugal, Ria Formosa Spoerner et al. 2012 Maribacter chungangensis CCUG 61948T JN036550 Undaria pinnatifida Korea, Jeju Island Weerawongwiwat et al. 2013 Maribacter arcticus DSM 23546T AY771762 Marine sediment Norway, Spitsbergen, Ny-Ålesund Cho et al. 2008 emend, Weerawongwiwat et al. 2013 Maribacter sedimenticola DSM 19840T AY271623 Bottom sediment sample Sea of Japan, Gulf of Peter the Nedashkovskaya et al. 2004a Great Maribacter stanieri DSM 19891T EU246691 Ulva fenestrata Russia, Sea of Japan, Gulf of Peter Nedashkovskaya et al. 2010 the Great, Troitsa Bay Maribacter ulvicola DSM 15366T AY271626 U. fenestrata Russia Nedashkovskaya et al. 2004a Maribacter polysiphoniae DSM 23514T AM497875 Polysiphonia japonica Russia, Sea of Japan, Gulf of Peter Nedashkovskaya et al. 2007 the Great, Troitsa Bay Algibacter lectus DSM 15365T AY187689 U. fenestrata Russia Nedashkovskaya et al. 2004c Ulvibacter litoralis DSM 16195T AY243096 U. fenestrata Russia, Sea of Japan, Gulf of Peter Nedashkovskaya et al. 2004b A. Weiss et al.: Morphogenesis
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