Publications

Publications in peer reviewed journals

11 Publications found
  • Omics research on abalone (Haliotis spp.): Current state and perspectives

    Nguyen TV, Alfaro AC, Mundy C, Petersen JM, Ragg NLC
    2022 - Aquaculture, 547: 737438

    Abstract: 

    The steady increase in abalone aquaculture production throughout the world has attracted growing interest in the application of new technologies, such as omics approaches for abalone research. Many omics techniques, such as genomics, transcriptomics, proteomics, and metabolomics are becoming established in abalone research and are beginning to reveal key molecules and pathways underlying many biological processes, and to identify associated candidate biomarkers of biological or environmental processes. In this contribution, we synthesize the published omics studies on abalone to highlight the current state of knowledge, open questions, and future directions. In addition, we outline the challenges and limitations of each omics field, some of which could be overcome by integrating multiple omics approaches – a future strategy with great potential for contributing to improve abalone production. Full text

  • Defensive symbiosis against giant viruses in amoebae

    Arthofer P, Delafont V, Willemsen A, Panhölzl F, Horn M
    2022 - PNAS, 119: e2205856119

    Abstract: 

    Protists are important regulators of microbial communities and key components in food webs with impact on nutrient cycling and ecosystem functioning. In turn, their activity is shaped by diverse intracellular parasites, including bacterial symbionts and viruses. Yet, bacteria–virus interactions within protists are poorly understood. Here, we studied the role of bacterial symbionts of free-living amoebae in the establishment of infections with nucleocytoplasmic large DNA viruses (Nucleocytoviricota). To investigate these interactions in a system that would also be relevant in nature, we first isolated and characterized a giant virus (Viennavirus, family Marseilleviridae) and a sympatric potential Acanthamoeba host infected with bacterial symbionts. Subsequently, coinfection experiments were carried out, using the fresh environmental isolates as well as additional amoeba laboratory strains. Employing fluorescence in situ hybridization and qPCR, we show that the bacterial symbiont, identified as Parachlamydia acanthamoebae, represses the replication of the sympatric Viennavirus in both recent environmental isolates as well as Acanthamoeba laboratory strains. In the presence of the symbiont, virions are still taken up, but viral factory maturation is inhibited, leading to survival of the amoeba host. The symbiont also suppressed the replication of the more complex Acanthamoeba polyphaga mimivirus and Tupanvirus deep ocean (Mimiviridae). Our work provides an example of an intracellular bacterial symbiont protecting a protist host against virus infections. The impact of virus–symbiont interactions on microbial population dynamics and eventually ecosystem processes requires further attention.

  • Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants

    Nepel M, Pfeifer J, Oberhauser FB, Richter A, Woebken D, Mayer VE
    2022 - BMC Biology, 20: 135

    Abstract: 

    Background: Symbiotic ant-plant associations, in which ants live on plants, feed on plant-provided food, and protect host trees against threats, are ubiquitous across the tropics, with the Azteca-Cecropia associations being amongst the most widespread interactions in the Neotropics. Upon colonization of Cecropia’s hollow internodes, Azteca queens form small patches with plant parenchyma, which are then used as waste piles when the colony grows. Patches—found in many ant-plant mutualisms—are present throughout the colony life cycle and may supplement larval food. Despite their initial nitrogen (N)-poor substrate, patches in Cecropia accommodate fungi, nematodes, and bacteria. In this study, we investigated the atmospheric N2 fixation as an N source in patches of early and established ant colonies. Results: Via 15N2 tracer assays, N2 fixation was frequently detected in all investigated patch types formed by three Azteca ant species. Quantified fixation rates were similar in early and established ant colonies and higher than in various tropical habitats. Based on amplicon sequencing, the identified microbial functional guild—the diazotrophs—harboring and transcribing the dinitrogenase reductase (nifH) gene was highly diverse and heterogeneous across Azteca colonies. The community composition differed between early and established ant colonies and partly between the ant species. Conclusions: Our data show that N2 fixation can result in reasonable amounts of N in ant colonies, which might not only enable bacterial, fungal, and nematode growth in the patch ecosystems but according to our calculations can even support the growth of ant populations. The diverse and heterogeneous diazotrophic community implies a functional redundancy, which could provide the ant-plant-patch system with a higher resilience towards changing environmental conditions. Hence, we propose that N2 fixation represents a previously unknown potential to overcome N limitations in arboreal ant colonies.

  • Ecology and evolution of chlamydial symbionts of arthropods

    Halter T, Koestlbacher S, Collingro A, Sixt BS, Toenshoff ER, Hendrickx F, Kostanjšek R, Horn M
    2022 - ISME Commun., 2: 45

    Abstract: 

    The phylum Chlamydiae consists of obligate intracellular bacteria including major human pathogens and diverse environmental representatives. Here we investigated the Rhabdochlamydiaceae, which is predicted to be the largest and most diverse chlamydial family, with the few described members known to infect arthropod hosts. Using published 16S rRNA gene sequence data we identified at least 388 genus-level lineages containing about 14 051 putative species within this family. We show that rhabdochlamydiae are mainly found in freshwater and soil environments, suggesting the existence of diverse, yet unknown hosts. Next, we used a comprehensive genome dataset including metagenome assembled genomes classified as members of the family Rhabdochlamydiaceae, and we added novel complete genome sequences of Rhabdochlamydia porcellionis infecting the woodlouse Porcellio scaber, and of 'Candidatus R. oedothoracis' associated with the linyphiid dwarf spider Oedothorax gibbosus. Comparative analysis of basic genome features and gene content with reference genomes of well-studied chlamydial families with known host ranges, namely Parachlamydiaceae (protist hosts) and Chlamydiaceae (human and other vertebrate hosts) suggested distinct niches for members of the Rhabdochlamydiaceae. We propose that members of the family represent intermediate stages of adaptation of chlamydiae from protists to vertebrate hosts. Within the genus Rhabdochlamydia, pronounced genome size reduction could be observed (1.49-1.93 Mb). The abundance and genomic distribution of transposases suggests transposable element expansion and subsequent gene inactivation as a mechanism of genome streamlining during adaptation to new hosts. This type of genome reduction has never been described before for any member of the phylum Chlamydiae. This study provides new insights into the molecular ecology, genomic diversity, and evolution of representatives of one of the most divergent chlamydial families.

  • Microbes From Mum: Symbiont transmission in the tropical reef sponge Ianthella basta

    Engelberts JP, Wahab MAA, Maldonado M, Rix L, Marangon E, Robbins SJ, Wagner M, Webster NS
    2022 - ISME Commun, in press

    Abstract: 

    Most marine sponge species harbour distinct communities of microorganisms which contribute to various aspects of their host’s health and physiology. In addition to their key roles in nutrient transformations and chemical defence, these symbiotic microbes may shape sponge phenotype by mediating important developmental stages and influencing the environmental tolerance of the host. However, the characterisation of each microbial taxa throughout a sponge’s life cycle remains challenging, with several sponge species hosting up to 3 000 distinct microbial species. Ianthella basta, an abundant broadcast spawning species in the Indo-Pacific is an emerging model for sponge symbiosis research as it harbours only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium. Here, we successfully spawned Ianthella basta, characterised its mode of reproduction, and used 16S rRNA gene amplicon sequencing, fluorescence in situ hybridisation, and transmission electron microscopy to characterise the microbial community throughout its life cycle. We confirmed I. basta as being gonochoric and showed that the three dominant symbionts, which together make up >90% of the microbiome according to 16S rRNA gene abundance, are vertically transmitted from mother to offspring by a unique method involving encapsulation in the peri-oocytic space, suggesting an obligate relationship between these microbes and their host.

  • Multi-strain probiotics show increased protection of intestinal epithelial cells against pathogens in rainbow trout (Oncorhynchus mykiss)

    Pillinger M, Weber B, Standen B, Schmid MC, Kesselring JC
    2022 - Aquaculture, 560: 738487

    Abstract: 

    The use of antibiotics to treat bacterial infections in aquaculture facilities adversely affects fish and environmental health, motivating the search for alternative products such as probiotics. The present study investigated the immune modulatory effects of inoculating the intestinal epithelial cells of rainbow trout (Oncorhynchus mykiss) with the probiotic bacteria Enterococcus faeciumPediococcus acidilacticiLactobacillus reuteri, and Bacillus subtilis alone (single-strains) or as mixtures, which either include or exclude B. subtilis (PWBsubtilis or PWOBsubtilis, respectively). To this end, isolated intestinal epithelial cells were either incubated without probiotics or with the single- or multi-strain probiotics and then challenged with common pathogens in aquaculture. The adhesion of probiotic and pathogenic bacteria to the intestinal cells was examined by flow cytometry and confocal microscopy and the relative expression of pro- and anti-inflammatory cytokine genes was assessed through quantitative real-time PCR. Although the highest inhibition of pathogen adhesion was observed for L. reuteri alone (88%), PWOBsubtilis and PWBsubtilis inhibited 77% and 71% of pathogen attachment, respectively. Single- and multi-strain probiotics were able to elicit an immune response by activation of both pro-inflammatory and anti-inflammatory cytokines production in rainbow trout intestinal epithelial cells. This expression was generally highest for multi-strain probiotics, particularly for PWBsubtilis. The tested probiotics present different modes of action, considering their inhibition capability and immunomodulatory effects. Hence the use of multi-strain products may promote a wider range of synergies on pathogens invasion and inhibition, and immunomodulatory effects that can represent an advantage to disease outbreaks prevention in rainbow trout production.

  • CT295 Is Chlamydia trachomatis’ phosphoglucomutase and a type 3 secretion substrate

    Triboulet A, N’Gadjaga MD, Niragire B, Köstlbacher S, Horn M, Aimanianda V, Subtil A
    2022 - Front Cell Infect Microbiol, 12: 866729

    Abstract: 

    The obligate intracellular bacteria Chlamydia trachomatis store glycogen in the lumen of the vacuoles in which they grow. Glycogen catabolism generates glucose-1-phosphate (Glc1P), while the bacteria can take up only glucose-6-phosphate (Glc6P). We tested whether the conversion of Glc1P into Glc6P could be catalyzed by a phosphoglucomutase (PGM) of host or bacterial origin. We found no evidence for the presence of the host PGM in the vacuole. Two C. trachomatis proteins, CT295 and CT815, are potential PGMs. By reconstituting the reaction using purified proteins, and by complementing PGM deficient fibroblasts, we demonstrated that only CT295 displayed robust PGM activity. Intriguingly, we showed that glycogen accumulation in the lumen of the vacuole of a subset of Chlamydia species (C. trachomatis, C. muridarum, C. suis) correlated with the presence, in CT295 orthologs, of a secretion signal recognized by the type three secretion (T3S) machinery of Shigella. C. caviae and C. pneumoniae do not accumulate glycogen, and their CT295 orthologs lack T3S signals. In conclusion, we established that the conversion of Glc1P into Glc6P was accomplished by a bacterial PGM, through the acquisition of a T3S signal in a “housekeeping” protein. Acquisition of this signal likely contributed to shaping glycogen metabolism within Chlamydiaceae.

  • Sulfur in lucinid bivalves inhibits intake rates of a molluscivore shorebird

    Tim Oortwijn, Jimmy de Fouw, Jillian Petersen, Jan A. van Gils
    2022 - Oecologia, in press

    Abstract: 

    A forager’s energy intake rate is usually constrained by a combination of handling time, encounter rate and digestion rate. On top of that, food intake may be constrained when a forager can only process a maximum amount of certain toxic compounds. The latter constraint is well described for herbivores with a limited tolerance to plant secondary metabolites. In sulfidic marine ecosystems, many animals host chemoautotrophic endosymbionts, which store sulfur compounds as an energy resource, potentially making their hosts toxic to predators. The red knot Calidris canutus canutus is a molluscivore shorebird that winters on the mudflats of Banc d’Arguin, where the most abundant bivalve prey Loripes orbiculatus hosts sulfide-oxidizing bacteria. In this system, we studied the potential effect of sulfur on the red knots’ intake rates, by offering Loripes with various sulfur content to captive birds. To manipulate toxicity, we starved Loripes for 10 days by removing them from their symbiont’s energy source sulfide. As predicted, we found lower sulfur concentrations in starved Loripes. We also included natural variation in sulfur concentrations by offering Loripes collected at two different locations. In both cases lower sulfur levels in Loripes resulted in higher consumption rates in red knots. Over time the red knots increased their intake rates on Loripes, showing their ability to adjust to a higher intake of sulfur.

  • Individual Sweet Taste Perception Influences Salivary Characteristics After Orosensory Stimulation With Sucrose and Noncaloric Sweeteners.

    Karl CM, Vidakovic A, Pjevac P, Hausmann B, Schleining G, Ley JP, Berry D, Hans J, Wendelin M, König J, Somoza V, Lieder B
    2022 - Front Nutr, 831726

    Abstract: 

    Emerging evidence points to a major role of salivary flow and viscoelastic properties in taste perception and mouthfeel. It has been proposed that sweet-tasting compounds influence salivary characteristics. However, whether perceived differences in the sensory properties of structurally diverse sweet-tasting compounds contribute to salivary flow and saliva viscoelasticity as part of mouthfeel and overall sweet taste perception remains to be clarified. In this study, we hypothesized that the sensory diversity of sweeteners would differentially change salivary characteristics in response to oral sweet taste stimulation. Therefore, we investigated salivary flow and saliva viscoelasticity from 21 healthy test subjects after orosensory stimulation with sucrose, rebaudioside M (RebM), sucralose, and neohesperidin dihydrochalcone (NHDC) in a crossover design and considered the basal level of selected influencing factors, including the basal oral microbiome. All test compounds enhanced the salivary flow rate by up to 1.51 ± 0.12 g/min for RebM compared to 1.10 ± 0.09 g/min for water within the 1st min after stimulation. The increase in flow rate was moderately correlated with the individually perceived sweet taste ( = 0.3, < 0.01) but did not differ between the test compounds. The complex viscosity of saliva was not affected by the test compounds, but the analysis of covariance showed that it was associated ( < 0.05) with mucin 5B (Muc5B) concentration. The oral microbiome was of typical composition and diversity but was strongly individual-dependent (permutational analysis of variance (PERMANOVA): = 0.76, < 0.001) and was not associated with changes in salivary characteristics. In conclusion, this study indicates an impact of individual sweet taste impressions on the flow rate without measurable changes in the complex viscosity of saliva, which may contribute to the overall taste perception and mouthfeel of sweet-tasting compounds.

  • Lipid synthesis at the trophic base as the source for energy management to build complex structures.

    Schnorr SL, Berry D
    2022 - Curr Opin Biotechnol, 364-373

    Abstract: 

    The review explores the ecological basis for bacterial lipid metabolism in marine and terrestrial ecosystems. We discuss ecosystem stressors that provoked early organisms to modify their lipid membrane structures, and where these stressors are found across a variety of environments. A major role of lipid membranes is to manage cellular energy utility, including how energy is used for signal propagation. As different environments are imbued with properties that necessitate variation in energy regulation, bacterial lipid synthesis has undergone incalculable permutations of functional trial and error. This may hold clues for how biotechnology can improvise a short-hand version of the evolutionary gauntlet to stimulate latent functional competences for the synthesis of rare lipids. Reducing human reliance on marine resources and deriving solutions for production of essential nutrients is a pressing problem in sustainable agriculture and aquaculture, as well as timely considering the increasing fragility of human health in an aging population.

  • Evolutionarily recent dual obligatory symbiosis among adelgids indicates a transition between fungus- and insect-associated lifestyles.

    Szabó G, Schulz F, Manzano-Marín A, Toenshoff ER, Horn M
    2022 - ISME J, 1: 247-256

    Abstract: 

    Adelgids (Insecta: Hemiptera: Adelgidae) form a small group of insects but harbor a surprisingly diverse set of bacteriocyte-associated endosymbionts, which suggest multiple replacement and acquisition of symbionts over evolutionary time. Specific pairs of symbionts have been associated with adelgid lineages specialized on different secondary host conifers. Using a metagenomic approach, we investigated the symbiosis of the Adelges laricis/Adelges tardus species complex containing betaproteobacterial ("Candidatus Vallotia tarda") and gammaproteobacterial ("Candidatus Profftia tarda") symbionts. Genomic characteristics and metabolic pathway reconstructions revealed that Vallotia and Profftia are evolutionary young endosymbionts, which complement each other's role in essential amino acid production. Phylogenomic analyses and a high level of genomic synteny indicate an origin of the betaproteobacterial symbiont from endosymbionts of Rhizopus fungi. This evolutionary transition was accompanied with substantial loss of functions related to transcription regulation, secondary metabolite production, bacterial defense mechanisms, host infection, and manipulation. The transition from fungus to insect endosymbionts extends our current framework about evolutionary trajectories of host-associated microbes.

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