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Frankobactin Metallophores Produced by Nitrogen-Fixing Frankia Actinobacteria Function in Toxic Metal Sequestration.

Abstract (Expand)

A series of new metallophores, referred to as frankobactins, were extracted from cultures of the symbiotic and nitrogen-fixing actinobacterium Frankia sp. CH37. Structure elucidation revealed a … 2-hydroxyphenyl-substituted oxazoline core and a chain composed of five proteinogenic and nonproteinogenic amino acids, suggesting nonribosomal peptide synthesis as the biosynthetic origin. By whole-genome sequencing, bioinformatic analysis, and comparison with other Frankia strains, the genetic locus responsible for the biosynthesis was detected. Spectrophotometric titration of frankobactin with Fe(III) and Cu(II) and mass spectrometry established the 1:1 (metal:frankobactin) coordination. Uptake experiments suggested that frankobactin A1 (1) did not serve to recruit iron, but to detoxify Cu(II). As frankobactin A1 prevents the cellular entry of Cu(II), it could play a crucial role in the symbiosis of Frankia sp. and its host in the reclamation of copper-contaminated soil.

Authors: J. F. Mohr, F. Baldeweg, M. Deicke, C. F. Morales-Reyes, D. Hoffmeister, T. Wichard

Date Published: 23rd Apr 2021

Publication Type: Journal

Rhizobactin B is the preferred siderophore by a novel Pseudomonas isolate to obtain iron from dissolved organic matter in peatlands.

Abstract (Expand)

Bacteria often release diverse iron-chelating compounds called siderophores to scavenge iron from the environment for many essential biological processes. In peatlands, where the biogeochemical cycle … of iron and dissolved organic matter (DOM) are coupled, bacterial iron acquisition can be challenging even at high total iron concentrations. We found that the bacterium Pseudomonas sp. FEN, isolated from an Fe-rich peatland in the Northern Bavarian Fichtelgebirge (Germany), released an unprecedented siderophore for its genus. High-resolution mass spectrometry (HR-MS) using metal isotope-coded profiling (MICP), MS/MS experiments, and nuclear magnetic resonance spectroscopy (NMR) identified the amino polycarboxylic acid rhizobactin and a novel derivative at even higher amounts, which was named rhizobactin B. Interestingly, pyoverdine-like siderophores, typical for this genus, were not detected. With peat water extract (PWE), studies revealed that rhizobactin B could acquire Fe complexed by DOM, potentially through a TonB-dependent transporter, implying a higher Fe binding constant of rhizobactin B than DOM. The further uptake of Fe-rhizobactin B by Pseudomonas sp. FEN suggested its role as a siderophore. Rhizobactin B can complex several other metals, including Al, Cu, Mo, and Zn. The study demonstrates that the utilization of rhizobactin B can increase the Fe availability for Pseudomonas sp. FEN through ligand exchange with Fe-DOM, which has implications for the biogeochemical cycling of Fe in this peatland.

Authors: S. Kugler, R. E. Cooper, J. Boessneck, K. Kusel, T. Wichard

Date Published: 7th Oct 2020

Publication Type: Journal

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

Abstract (Expand)

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.

Authors: T. Alsufyani, G. Califano, M. Deicke, J. Grueneberg, A. Weiss, A. H. Engelen, M. Kwantes, J. F. Mohr, J. F. Ulrich, T. Wichard

Date Published: 11th Jun 2020

Publication Type: Journal

Metallophore profiling of nitrogen-fixing Frankia spp. to understand metal management in the rhizosphere of actinorhizal plants.

Abstract (Expand)

Frankia spp. are widespread nitrogen-fixing soil bacteria, which often live in symbiosis with a broad range of hosts. Metal homeostasis plays a crucial role in the success of the symbiosis regarding … the acquisition of essential trace metals and detoxification of potentially toxic elements. We have hypothesised that Frankia releases many organic ligands with a broad spectrum of affinity for essential and toxic metals. We coined the term 'ligandosphere' to describe the entirety of excreted metal complexing agents and ligands derived from the dissolved organic matter. Using metal isotope-coded profiling (MICP); metallophores of physiological important and toxic trace metals were identified by the addition of stable metal isotope pairs such as 54Fe/58Fe, 63Cu/65Cu, 66Zn/68Zn or 95Mo/98Mo. Liquid chromatography coupled to a mass spectrometer revealed strong variations of the metallophore profile in between the 14 test-strains. In total, about 83 organic ligands were identified as binding to one of the tested metals. The predicted sum formula of the major Fe binding ligands and MS/MS experiments suggested that several metallophore candidates have a similar molecular backbone. Growth experiments with a hyper-producer of metallophores revealed a positive relationship between metallophore production and the concentration of Cu in the growth medium. The present study provides the first comprehensive overview of the complexity of Frankia's ligandosphere. It opens a path to a deeper understanding of mechanisms that regulate metal homeostasis in frankiae. Deciphering these mechanisms is important since the fitness of actinorhizal plants and their potential in ecological restoration relies heavily on their symbiosis with frankiae.

Authors: M. Deicke, J. F. Mohr, S. Roy, P. Herzsprung, J. P. Bellenger, T. Wichard

Date Published: 17th Apr 2019

Publication Type: Journal

Algae induce siderophore biosynthesis in the freshwater bacterium Cupriavidus necator H16.

Abstract (Expand)

Cupriachelin is a photoreactive lipopeptide siderophore produced by the freshwater bacterium Cupriavidus necator H16. In the presence of sunlight, the iron-loaded siderophore undergoes photolytic … cleavage, thereby releasing solubilized iron into the environment. This iron is not only available to the siderophore producer, but also to the surrounding microbial community. In this study, the cupriachelin-based interaction between C. necator H16 and the freshwater diatom Navicula pelliculosa was investigated. A reporter strain of the bacterium was constructed to study differential expression levels of the cupriachelin biosynthesis gene cucJ in response to varying environmental conditions. Not only iron starvation, but also culture supernatants of N. pelliculosa were found to induce cupriachelin biosynthesis. The transcription factors involved in this differential gene expression were identified using DNA-protein pulldown assays. Besides the well-characterized ferric uptake regulator, a two-component system was found to tune the expression of cupriachelin biosynthesis genes in the presence of diatom supernatants.

Authors: C. Kurth, I. Wasmuth, T. Wichard, G. Pohnert, M. Nett

Date Published: 27th Nov 2018

Publication Type: Journal

Conspecificity of the model organism Ulva mutabilis and Ulva compressa (Ulvophyceae, Chlorophyta).

Abstract (Expand)

As one of the most abundant and ubiquitous representatives of marine and brackish coastal macrophytobenthos communities, the genus Ulva is not only an important primary producer but also of ecological … and morphogenetic interest to many scientists. Ulva mutabilis became an important model organism to study morphogenesis and mutualistic interactions of macroalgae and microorganisms. Here, we report that our collections of Ulva compressa Linnaeus (1753) from Germany are conspecific with the type strains of the model organism U. mutabilis Foyn (1958), which were originally collected at Olhao on the south coast of Portugal and have from that time on been maintained in culture as gametophytic and parthenogenetic lab strains. Different approaches were used to test conspecificity: (i) comparisons of vegetative and reproductive features of cultured material of U. mutabilis and German U. compressa demonstrated a shared morphological pattern; (ii) gametes of U. compressa and U. mutabilis successfully mated and developed into fertile sporophytic first-generation offspring; (iii) molecular phylogenetics and species delimitation analyses based on the Generalized Mixed Yule-Coalescent method showed that U. mutabilis isolates (sl-G[mt+]) and (wt-G[mt-]) and U. compressa belong to a unique Molecular Operational Taxonomic Unit. According to these findings, there is sufficient evidence that U. mutabilis and U. compressa should be regarded as conspecific.

Authors: S. Steinhagen, A. Barco, T. Wichard, F. Weinberger

Date Published: 28th Oct 2018

Publication Type: Journal

Insights into the Evolution of Multicellularity from the Sea Lettuce Genome.

Abstract (Expand)

We report here the 98.5 Mbp haploid genome (12,924 protein coding genes) of Ulva mutabilis, a ubiquitous and iconic representative of the Ulvophyceae or green seaweeds. Ulva's rapid and abundant … growth makes it a key contributor to coastal biogeochemical cycles; its role in marine sulfur cycles is particularly important because it produces high levels of dimethylsulfoniopropionate (DMSP), the main precursor of volatile dimethyl sulfide (DMS). Rapid growth makes Ulva attractive biomass feedstock but also increasingly a driver of nuisance "green tides." Ulvophytes are key to understanding the evolution of multicellularity in the green lineage, and Ulva morphogenesis is dependent on bacterial signals, making it an important species with which to study cross-kingdom communication. Our sequenced genome informs these aspects of ulvophyte cell biology, physiology, and ecology. Gene family expansions associated with multicellularity are distinct from those of freshwater algae. Candidate genes, including some that arose following horizontal gene transfer from chromalveolates, are present for the transport and metabolism of DMSP. The Ulva genome offers, therefore, new opportunities to understand coastal and marine ecosystems and the fundamental evolution of the green lineage.

Authors: O. De Clerck, S. M. Kao, K. A. Bogaert, J. Blomme, F. Foflonker, M. Kwantes, E. Vancaester, L. Vanderstraeten, E. Aydogdu, J. Boesger, G. Califano, B. Charrier, R. Clewes, A. Del Cortona, S. D'Hondt, N. Fernandez-Pozo, C. M. Gachon, M. Hanikenne, L. Lattermann, F. Leliaert, X. Liu, C. A. Maggs, Z. A. Popper, J. A. Raven, M. Van Bel, P. K. I. Wilhelmsson, D. Bhattacharya, J. C. Coates, S. A. Rensing, D. Van Der Straeten, A. Vardi, L. Sterck, K. Vandepoele, Y. Van de Peer, T. Wichard, J. H. Bothwell

Date Published: 24th Sep 2018

Publication Type: Journal

Role of Chemical Mediators in Aquatic Interactions across the Prokaryote-Eukaryote Boundary.

Abstract (Expand)

There is worldwide growing interest in the occurrence and diversity of metabolites used as chemical mediators in cross-kingdom interactions within aquatic systems. Bacteria produce metabolites to protect … and influence the growth and life cycle of their eukaryotic hosts. In turn, the host provides a nutrient-enriched environment for the bacteria. Here, we discuss the role of waterborne chemical mediators that are responsible for such interactions in aquatic multi-partner systems, including algae or invertebrates and their associated bacteria. In particular, this review highlights recent advances in the chemical ecology of aquatic systems that support the overall ecological significance of signaling molecules across the prokaryote-eukaryote boundary (cross-kingdom interactions) for growth, development and morphogenesis of the host. We emphasize the value of establishing well-characterized model systems that provide the basis for the development of ecological principles that represent the natural lifestyle and dynamics of aquatic microbial communities and enable a better understanding of the consequences of environmental change and the most effective means of managing community interactions.

Authors: T. Wichard, C. Beemelmanns

Date Published: 15th Aug 2018

Publication Type: Journal

Gramibactin is a bacterial siderophore with a diazeniumdiolate ligand system.

Abstract (Expand)

Genome mining and chemical analyses revealed that rhizosphere bacteria (Paraburkholderia graminis) produce a new type of siderophore, gramibactin, a lipodepsipeptide that efficiently binds iron with a … logbeta value of 27.6. Complexation-induced proton NMR chemical shifts show that the unusual N-nitrosohydroxylamine (diazeniumdiolate) moieties participate in metal binding. Gramibactin biosynthesis genes are conserved in numerous plant-associated bacteria associated with rice, wheat, and maize, which may utilize iron from the complex.

Authors: R. Hermenau, K. Ishida, S. Gama, B. Hoffmann, M. Pfeifer-Leeg, W. Plass, J. F. Mohr, T. Wichard, H. P. Saluz, C. Hertweck

Date Published: 1st Aug 2018

Publication Type: Journal

DeltaMS: a tool to track isotopologues in GC- and LC-MS data

Abstract (Expand)

Introduction: Stable isotopic labeling experiments are powerful tools to study metabolic pathways, to follow tracers and fluxes in biotic and abiotic transformations and to elucidate molecules involved …d in metal complexing. Objective: To introduce a software tool for the identification of isotopologues from mass spectrometry data. Methods: DeltaMS relies on XCMS peak detection and X13CMS isotopologue grouping and then analyses data for specific isotope ratios and the relative error of these ratios. It provides pipelines for recognition of isotope patterns in three experiment types commonly used in isotopic labeling studies: (1) Search for isotope signatures with a specific mass shift and intensity ratio in one sample set. (2) Analyze two sample sets for a specific mass shift and, optionally, the isotope ratio, whereby one sample set is isotope-labeled, and one is not. (3) Analyze isotope-guided perturbation experiments with a setup described in X13CMS. Results: To illustrate the versatility of DeltaMS, we analyze data sets from case-studies that commonly pose challenges in evaluation of natural isotopes or isotopic signatures in labeling experiment. In these examples, the untargeted detection of sulfur, bromine and artificial metal isotopic patterns is enabled by the automated search for specific isotopes or isotope signatures. Conclusion: DeltaMS provides a platform for the identification of (pre-defined) isotopologues in MS data from single samples or comparative metabolomics data sets.

Authors: Tim U. H. Baumeister, Nico Ueberschaar, Wolfgang Schmidt-Heck, J. Frieder Mohr, Michael Deicke, Thomas Wichard, Reinhard Guthke, Georg Pohnert

Date Published: 27th Feb 2018

Publication Type: Not specified

Macroalgal-bacterial interactions: Role of dimethylsulfoniopropionate in microbial gardening by Ulva (Chlorophyta).

Abstract (Expand)

The marine macroalga Ulva mutabilis (Chlorophyta) develops into callus-like colonies consisting of undifferentiated cells and abnormal cell walls under axenic conditions. Ulva mutabilis is routinely … cultured with two bacteria, the Roseovarius sp. MS2 strain and the Maribacter sp. MS6 strain, which release morphogenetic compounds and ensure proper algal morphogenesis. Using this tripartite community as an emerging model system, we tested the hypothesis that the bacterial-algal interactions evolved as a result of mutually taking advantage of signals in the environment. Our study aimed to determine whether cross-kingdom crosstalk is mediated by the attraction of bacteria through algal chemotactic signals. Roseovarius sp. MS2 senses the known osmolyte dimethylsulfoniopropionate (DMSP) released by Ulva into the growth medium. Roseovarius sp. is attracted by DMSP and takes it up rapidly such that DMSP can only be determined in axenic growth media. As DMSP did not promote bacterial growth under the tested conditions, Roseovarius benefited solely from glycerol as the carbon source provided by Ulva. Roseovarius quickly catabolized DMSP into methanethiol (MeSH) and dimethylsulphide (DMS). We conclude that many bacteria can use DMSP as a reliable signal indicating a food source and promote the subsequent development and morphogenesis in Ulva.

Authors: R. W. Kessler, A. Weiss, S. Kuegler, C. Hermes, T. Wichard

Date Published: 2018

Publication Type: Journal

Bacteria-induced morphogenesis of Ulva intestinalis and Ulva mutabilis (Chlorophyta): a contribution to the lottery theory.

Abstract (Expand)

The green marine macroalgae of the class Ulvophyceae (Ulvophytes) are common algae distributed worldwide particularly in intertidal areas, which play a key role in aquatic ecosystems. They are potentially … valuable resources for food, animal feed and fuel but can also cause massive nuisance blooms. Members of Ulvaceae, like many other seaweeds, harbour a rich diversity of epiphytic bacteria with functions related to host growth and morphological development. In the absence of appropriate bacterially derived signals, germ cells of the genus Ulva develop into 'atypical' colonies consisting of undifferentiated cells with abnormal cell walls. This paper examines the specificity of bacteria-induced morphogenesis in Ulva, by cross-testing bacteria isolated from several Ulva species on two Ulva species, the emerging model system Ulva mutabilis and the prominent biofouler species Ulva intestinalis. We show that pairs of bacterial strains isolated from species other than U. mutabilis and U. intestinalis can fully rescue axenic plantlets generated either from U. mutabilis or U. intestinalis gametes. This laboratory-based study demonstrates that different compositions of microbial communities with similar functional characteristics can enable complete algal morphogenesis and thus supports the 'competitive lottery' theory for how symbiotic bacteria drive algal development.

Authors: F. Ghaderiardakani, J. C. Coates, T. Wichard

Date Published: 16th Aug 2017

Publication Type: Not specified

In situ monitoring of molecular changes during cell differentiation processes in marine macroalgae through mass spectrometric imaging.

Abstract (Expand)

Matrix-assisted laser desorption/ionization mass spectrometric imaging (MALDI-MSI) was employed to discriminate between cell differentiation processes in macroalgae. One of the key developmental processes … in the algal life cycle is the production of germ cells (gametes and zoids). The gametogenesis of the marine green macroalga Ulva mutabilis (Chlorophyta) was monitored by metabolomic snapshots of the surface, when blade cells differentiate synchronously into gametangia and giving rise to gametes. To establish MSI for macroalgae, dimethylsulfoniopropionate (DMSP), a known algal osmolyte, was determined. MSI of the surface of U. mutabilis followed by chemometric data analysis revealed dynamic metabolomic changes during cell differentiation. DMSP and a total of 55 specific molecular biomarkers, which could be assigned to important stages of the gametogenesis, were detected. Our research contributes to the understanding of molecular mechanisms underlying macroalgal cell differentiation. Graphical abstract Molecular changes during cell differentiation of the marine macroalga Ulva were visualized by matrix assisted laser desorption/ionization mass spectrometric imaging (MALDI-MSI).

Authors: R. W. Kessler, A. C. Crecelius, U. S. Schubert, T. Wichard

Date Published: 11th Jun 2017

Publication Type: Not specified

Time Course Exo-Metabolomic Profiling in the Green Marine Macroalga Ulva (Chlorophyta) for Identification of Growth Phase-Dependent Biomarkers

Abstract (Expand)

The marine green macroalga Ulva (Chlorophyta) lives in a mutualistic symbiosis with bacteria that influence growth, development, and morphogenesis. We surveyed changes in Ulva's chemosphere, which … was defined as a space where organisms interact with each other via compounds, such as infochemicals, nutrients, morphogens, and defense compounds. Thereby, Ulva mutabilis cooperates with bacteria, in particular, Roseovarius sp. strain MS2 and Maribacter sp. strain MS6 (formerly identified as Roseobacter sp. strain MS2 and Cytophaga sp. strain MS6). Without this accompanying microbial flora, U. mutabilis forms only callus-like colonies. However, upon addition of the two bacteria species, in effect forming a tripartite community, morphogenesis can be completely restored. Under this strictly standardized condition, bioactive and eco-physiologically-relevant marine natural products can be discovered. Solid phase extracted waterborne metabolites were analyzed using a metabolomics platform, facilitating gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry (LC-MS) analysis, combined with the necessary acquisition of biological metadata. Multivariate statistics of the GC-MS and LC-MS data revealed strong differences between Ulva's growth phases, as well as between the axenic Ulva cultures and the tripartite community. Waterborne biomarkers, including glycerol, were identified as potential indicators for algal carbon source and bacterial-algal interactions. Furthermore, it was demonstrated that U. mutabilis releases glycerol that can be utilized for growth by Roseovarius sp. MS2.

Authors: T. Alsufyani, A. Weiss, T. Wichard

Date Published: 12th Jan 2017

Publication Type: Not specified

Cell structure and microtubule organisation during gametogenesis of Ulva mutabilis Føyn (Chlorophyta)

Abstract (Expand)

Cell structure and microtubule organisation during gametogenesis of the green alga Ulva mutabilis was studied using light microscopy, transmission electron microscopy (TEM) and tubulin immunofluorescence. … Microtubules in vegetative cells are organised in parallel bundles traversing the cortical cytoplasm. During gametogenesis, induced blade cells are transformed to gametangia, depending on the maturity of the algae and the removal of regulatory sporulation inhibitors. This differentiation is accompanied by formation of a conical cell projection (papilla) towards the exterior of the thallus. Microtubules form a clear, basket-like configuration converging towards the conical tip, but not reaching it. The conical microtubule structure stops below the tip, leaving a circular “opening”. Parallel to the above, the cell wall of the tip is differentiated, forming a “cap”. Nuclear divisions start at this stage, finally forming the nuclei of future gametes. Cytokinesis takes place by membrane furrowing and vesicle fusion, giving rise to 16 oval-shaped gametes. The conical microtubule organisation is gradually depolymerised, and a cortical, intensely fluorescing microtubule bundle is formed in each gamete. At this stage, the cap at the conical cell wall projection is removed and the exit pore opens. The biflagellate gametes remain initially motionless, connected by thin cytoplasmic bridges. Finally, they are released to the environment upon additional removal of a swarming inhibitor accumulated in the growth medium during gametogenesis. Keywords: cell differentiation; gametogenesis; green macroalgae; immunofluorescence; microtubule cytoskeleton

Authors: Thomas Wichard, Christos Katsaros, Anne Weiss, Ira Llangos

Date Published: 11th Jan 2017

Publication Type: Not specified

A fast and direct liquid chromatography-mass spectrometry method to detect and quantify polyunsaturated aldehydes and polar oxylipins in diatoms

Abstract (Expand)

Polyunsaturated aldehydes (PUAs) are a group of microalgal metabolites that have attracted a lot of attention due to their biological activity. Determination of PUAs has become an important routine … procedure in plankton and biofilm investigations, especially those that deal with chemically mediated interactions. Here we introduce a fast and direct derivatization free method that allows quantifying PUAs in the nanomolar range, sufficient to undertake the analysis from cultures and field samples. The sample preparation requires one simple filtration step and the initiation of PUA formation by cell disruption. After centrifugation the samples are ready for measurement without any further handling. Within one chromatographic run this method additionally allows us to monitor the formation of the polar oxylipins arising from the cleavage of precursor fatty acids. The robust method is based on analyte separation and detection using ultra high performance liquid chromatography-atmospheric pressure chemical ionization mass spectrometry (UHPLC-APCI MS) and enables high throughput investigations by employing an analysis time of only 5 min. Our protocol thus provides an alternative and extension to existing PUA determinations based on gas chromatography-mass spectrometry (GC-MS) with shorter run times and without any chemical derivatization. It also enables researchers with widely available LC-MS analytical platforms to monitor PUAs. Additionally, non-volatile oxylipins such as ω-oxo-acids and related compounds can be elucidated and monitored.

Authors: Constanze Kuhlisch, Michael Deicke, Nico Ueberschaar, Thomas Wichard, Georg Pohnert

Date Published: 15th Oct 2016

Publication Type: Not specified

Bakterien-induzierte Morphogenese der marinen Makroalge Ulva

Abstract (Expand)

The morphogenesis of the marine green algae Ulva mutabilis depends on bacteria that release diffusible morphogenetic compounds. Axenic U. mutabilis gametes develop into callus-like colonies without … normal cell walls. From the accompanying microbial flora two specific bacteria were isolated, which form a symbiotic tripartite community and induce readily algal morphogenesis. We use axenic algal cultures as a powerful tool to investigate the multiple cross-kingdom interactions on a molecular level.

Author: Thomas Wichard

Date Published: 2nd Oct 2016

Publication Type: Not specified

Identification of Metallophores and Organic Ligands in the Chemosphere of the Marine Macroalga Ulva (Chlorophyta) and at Land-Sea Interfaces

Abstract (Expand)

The roles of organic matter in seawater have often been discussed from the aspect of metal toxicity and bioavailability in seawater. In fact, organic ligands, as part of the organic matter, can work … as a trace metal ion buffer system. At the same time, however, the release of well-defined metal chelators as exudates by, for example, marine bacteria is necessary to compete with natural metal complexes and sustain the metal acquisition required for several processes including nitrogen fixation. The identification, isolation, and structure elucidation of chelators is, thus, essential to our understanding of metal stress management in the natural habitat and role of these chelators on cellular process. The isolation of an organic ligand from its chemosphere is a challenging task. The purpose of this paper is, therefore, to give an additional perspective on how the effective application of stable isotope pairs of a metal of interest (both cations and oxoanions) combined with mass spectrometric analyses can pave the way to discovering new organic ligands (i.e., metallophores) and the chelating characteristics of dissolved organic matter (DOM): Pairs of isotopes, such as 54Fe and 58Fe (or any other pair of available isotopes of a given metal), can be used to create easily detectable unique isotopic signatures in mass spectra when they are bound by chelators. The identification of organic ligands is outlined for a proposed model system of mutualistic interactions between the green macroalga Ulva (Chlorophyta) and associated bacteria, as well as discussed briefly for DOM along land-sea gradients. Overall, the characterization of a broader spectrum of chelators in aquatic systems will open a new window to decipher the eco-physiological functions of organic ligands as a metal ion buffer and metallophores in metal cycling in marine ecosystems.

Author: Thomas Wichard

Date Published: 29th Jul 2016

Publication Type: Not specified

Macroalgal Morphogenesis Induced by Waterborne Compounds and Bacteria in Coastal Seawater

Abstract (Expand)

Axenic gametes of the marine green macroalga Ulva mutabilis Foyn (Ria Formosa, locus typicus) exhibit abnormal development into slow-growing callus-like colonies with aberrant cell walls. Under laboratory … conditions, it was previously demonstrated that all defects in growth and thallus development can be completely abolished when axenic gametes are inoculated with a combination of two specific bacterial strains originally identified as Roseobacter sp. strain MS2 and Cytophaga sp. strain MS6. These bacteria release diffusible morphogenetic compounds (= morphogens), which act similar to cytokinin and auxin. To investigate the ecological relevance of the waterborne bacterial morphogens, seawater samples were collected in the Ria Formosa lagoon (Algarve, Southern Portugal) at 20 sampling sites and tidal pools to assess their morphogenetic effects on the axenic gametes of U. mutabilis. Specifically the survey revealed that sterile-filtered seawater samples can completely recover growth and morphogenesis of U. mutabilis under axenic conditions. Morphogenetic activities of free-living and epiphytic bacteria isolated from the locally very abundant Ulva species (i.e., U. rigida) were screened using a multiwell-based testing system. The most represented genera isolated from U. rigida were Alteromonas, Pseudoalteromonas and Sulfitobacter followed by Psychrobacter and Polaribacter. Several naturally occurring bacterial species could emulate MS2 activity (= induction of cell divisions) regardless of taxonomic affiliation, whereas the MS6 activity (= induction of cell differentiation and cell wall formation) was species-specific and is probably a feature of difficult-to-culture bacteria. Interestingly, isolated bacteroidetes such as Algoriphagus sp. and Polaribacter sp. could individually trigger complete Ulva morphogenesis and thus provide a novel mode of action for bacterial-induced algal development. This study also highlights that the accumulation of algal growth factors in a shallow water body separated from the open ocean by barrier islands might have strong implications to, for example, the wide usage of natural coastal seawater in algal (land based) aquacultures of Ulva.

Authors: J. Grueneberg, A. H. Engelen, R. Costa,

Date Published: 8th Jan 2016

Publication Type: Not specified

Effect of organic matter on nitrogenase metal cofactors homeostasis in Azotobacter vinelandii under diazotrophic conditions

Abstract (Expand)

Biological nitrogen fixation can be catalyzed by three isozymes of nitrogenase: Mo-nitrogenase, V-nitrogenase and Fe-nitrogenase. The activity of these isozymes strongly depends on their metal cofactors, … Mo, V and Fe, and their bioavailability in ecosystems. Here, we show how metal bioavailability can be affected by the presence of tannic acid (organic matter), and the subsequent consequences on diazotrophic growth of the soil bacterium Azotobacter vinelandii. In the presence of tannic acids, A. vinelandii produces a higher amount of metallophores, which coincides with an active, regulated and concomitant acquisition of Mo and V under cellular conditions that are usually considered not Mo limiting. The associated nitrogenase genes exhibit decreased nifD expression and increased vnfD expression. Thus, in limiting bioavailable metal conditions, A. vinelandii takes advantage of its nitrogenase diversity to ensure optimal diazotrophic growth.

Authors: C. Jouogo Noumsi, N. Pourhassan, R. Darnajoux, , , V. Burrus, J. P. Bellenger

Date Published: 10th Nov 2015

Publication Type: Not specified

Transformation ofUlva mutabilis(Chlorophyta) by vector plasmids integrating into the genome

Abstract (Expand)

A method for the stable transformation of the green marine macroalga Ulva mutabilis was developed based on vector plasmids integrating into the genome. By combination of the expression signals (promoter, … enhancer, and transcriptional termination sequences) of a chromosomal rbcS gene from U. mutabilis with the bleomycin resistance gene (ble) from Streptoalloteichus hindustanus, a dominant selectable marker gene was constructed for the preparation of a series of E. coli—U. mutabilis shuttle vector plasmids. Special vectors were prepared for the introduction and expression of foreign genes in Ulva, for insertional mutagenesis and gene tagging by plasmid integration into the genome, and for protein tagging by the green fluorescent protein, as well as tools for posttranscriptional gene silencing and cosmid cloning to prepare genomic gene libraries for mutant gene complementation. The vectors were successfully tested in pilot experiments, where they were efficiently introduced into Ulva gametes, zoospores or protoplasts of somatic blade cells by treatment with Ca2+-ions and polyethylene glycol under isotonic conditions at low ionic strength. The parthenogenetically propagated phleomycin-resistant transformants of the mutant slender (sl) and the wildtype (wt) were demonstrated to be carrying the plasmids randomly integrated into the chromosomes often as tandem repeat clusters.

Authors: Wolfgang Oertel, Thomas Wichard, Adelheid Weissgerber

Date Published: 18th Sep 2015

Publication Type: Not specified

The green seaweed Ulva: a model system to study morphogenesis

Abstract (Expand)

Green macroalgae, mostly represented by the Ulvophyceae, the main multicellular branch of the Chlorophyceae, constitute important primary producers of marine and brackish coastal ecosystems. Ulva or … sea lettuce species are some of the most abundant representatives, being ubiquitous in coastal benthic communities around the world. Nonetheless the genus also remains largely understudied. This review highlights Ulva as an exciting novel model organism for studies of algal growth, development and morphogenesis as well as mutualistic interactions. The key reasons that Ulva is potentially such a good model system are: (i) patterns of Ulva development can drive ecologically important events, such as the increasing number of green tides observed worldwide as a result of eutrophication of coastal waters, (ii) Ulva growth is symbiotic, with proper development requiring close association with bacterial epiphytes, (iii) Ulva is extremely developmentally plastic, which can shed light on the transition from simple to complex multicellularity and (iv) Ulva will provide additional information about the evolution of the green lineage.

Authors: , B. Charrier, F. Mineur, J. H. Bothwell, O. D. Clerck, J. C. Coates

Date Published: 19th Feb 2015

Publication Type: Not specified

Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): comparison with Ulva mutabilis and potential for laboratory culture

Abstract (Expand)

Green Ulvophyte macroalgae represent attractive model systems for understanding growth, development, and evolution. They are untapped resources for food, fuel, and high-value compounds, but can also … form nuisance blooms. To fully analyze green seaweed morphogenesis, controlled laboratory-based culture of these organisms is required. To date, only a single Ulvophyte species, Ulva mutabilis Foyn, has been manipulated to complete its whole life cycle in laboratory culture and to grow continuously under axenic conditions. Such cultures are essential to address multiple key questions in Ulva development and in algal-bacterial interactions. Here we show that another Ulva species, U. linza, with a broad geographical distribution, has the potential to be grown in axenic culture similarly to U. mutabilis. U. linza can be reliably induced to sporulate (form gametes and zoospores) in the laboratory, by cutting the relevant thallus tissue into small pieces and removing extracellular inhibitors (sporulation and swarming inhibitors). The germ cells work as an ideal feed stock for standardized algae cultures. The requirement of U. linza for bacterial signals to induce its normal morphology (particularly of the rhizoids) appears to have a species-specific component. The axenic cultures of these two species pave the way for future comparative studies of algal-microbial interactions.

Authors: E. F. Vesty, R. W. Kessler, , J. C. Coates

Date Published: 26th Jan 2015

Publication Type: Not specified

Morphogenesis of Ulva mutabilis (Chlorophyta) induced by Maribacter species (Bacteroidetes, Flavobacteriaceae)

Abstract (Expand)

Growth and morphogenesis of the sea lettuce Ulva (Chlorophyta) depends on the combination of regulative morphogenetic compounds released by specific associated bacteria. Axenic Ulva gametes develop … parthenogenetically into callus-like colonies consisting of undifferentiated cells without normal cell walls. In Ulva mutabilis Føyn, two bacterial strains, Maribacter sp. strain MS6 and Roseovarius strain MS2, can restore the complete algal morphogenesis forming a tripartite symbiotic community. Morphogenetic compounds (=morphogens) released by the MS6-strain induce rhizoid formation and cell wall development in U. mutabilis, while several bacteria of the Roseobacter clade, including the MS2-strain, promote blade cell division and thallus elongation. In this study, 12 type strains of the Flavobacteriaceae family, including six Maribacter strains, were examined for their morphogenetic activity in comparison to the original MS6-strain isolated from U. mutabilis. The bioassay is based on the functional complementation of the tested Flavobacteriaceae strain with the Roseovarius MS2-strain. If the test-strain possesses morphogenetic activity complementary to the factor of the MS2-strain, the complete morphogenesis of U. mutabilis can be restored. This bioassay revealed not only the stand-alone activity of certain bacteria, but also their essential capability to take part in the orchestrated bacteria-induced morphogenesis of U. mutabilis. All Maribacter type strains isolated from Ulva could phenocopy the MS6-strain, whereas some distantly related Flavobacteriaceae and a Maribacter strain isolated from a red alga did not possess any activity. Keywords: bacteroidetes; cell differentiation; green macroalga; morphogens; thallusin

Authors: Thomas Wichard, Anne Weiss, R. Costa

Date Published: No date defined

Publication Type: Not specified

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