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Reusch, T. B. H.

Publications and source records attributed to Reusch, T. B. H..

At least 19 recordsLinked to original sources

Comparative somatic genomics reveals divergent development of cell lineages across scleractinian corals

Somatic mutations may drive adaptation and aging across diverse life forms, yet their role remains poorly understood in many early-branching animals. Here, we compare somatic mutation accumulation in the robust coral Orbicella faveolata with previous findings in the complex coral Acropora palmata. Whole-genome sequencing revealed high fixation of somatic genetic variants in O. faveolata, particularly in older, interior regions of colonies--contrasting with A. palmata. These patterns suggest distinct cell population dynamics between clades, indicating a segregated, mammal-like germline in O. faveolata, whereas such a germline remains undetected in A. palmata. This underscores the diversity of somatic evolutionary mechanisms across scleractinian corals.

genomics↗

Phylogeny-aware comparative genomics of Vibrio vulnificus links genetic traits to pathogenicity

Vibrio vulnificus is a natural inhabitant of coastal brackish waters worldwide and an opportunistic pathogen that can cause severe infections and septicemia through seafood consumption or wound exposure. Due to global warming, its abundance is increasing at high latitudes. While the species harbors diverse virulence factors, its precise disease mechanisms remain unclear. Comparative genomics between clinical and environmental isolates can help identify key virulence genes, but the limited availability of genomes from environmental isolates has hindered progress. In this study, we sequenced the genomes of 82 V. vulnificus isolates from water, sediment, and seagrass along the Baltic Sea coast and complemented with published genomes from 208 clinical and 117 globally distributed isolates for comparative analysis. Phylogenetic reconstruction confirmed four major lineages, with Baltic Sea strains confined to lineage L2 and L4, while clinical and environmental strains were distributed across all lineages. This suggests that the phylogenetic structure of V. vulnificus reflects adaptation to environmental conditions rather than pathogenicity. Using the PhyloBOTL pipeline developed here, we identified 128 orthologs significantly enriched in clinical isolates, grouped into 36 co-localization clusters based on proximity in the genomes. These included genes linked to virulence, such as those for capsular polysaccharide synthesis and biofilm formation, as well as previously unrecognized candidates, including chaperone-usher pilus biosynthesis, spermidine synthesis, Type VI secretion effectors, and an RTX toxin-like protein. Several of the clinically enriched gene clusters have been independently lost in three V. vulnificus clades, suggesting convergent evolution and a distinct ecological niche shared by these claded. Finally, we used the clinically enriched genes to design PCR primers for detecting and monitoring pathogenic V. vulnificus strains, providing a valuable tool for surveillance and public health efforts.

microbiology↗

Mosaic accumulation of somatic genetic variation and estimates of age in the long-lived reef-building coral Acropora palmata

Somatic genetic variation (SOGV), accumulating during an organisms lifetime, was traditionally viewed as detrimental rather than adaptive due to links with cancer and senescence. However, in modular organisms like corals, deleterious mutations can be purged at the cellular or polyp level, while adaptive mutations may rise in frequency as polyps create genetically distinct modules. Quantifying the somatic genetic landscape in corals is necessary to understand the role these mutations may have in coral and clonal animal development and evolution. Here, we catalog somatic genetic variation in eight Acropora palmata colonies from Curacao. Whole genomes were sequenced (70-100x depth), documenting mutation variant allele frequency shifts as genets aged. Large numbers of SOGVs were observed in six- to ten-year-old colonies, and inferred mutation rates were used to age a genet of uncertain age to almost a century old. Although mutations were not fixed at the polyp or branch levels, i.e. they always displayed frequencies <0.5 as expected at mutating homozygous sites, their allele frequencies followed a power-law distribution, similar to aging human tissues. No signs of positive selection were found; instead SOGVs in the colony of uncertain age were under purifying selection. In one colony, mutations in 28 samples from along a branch were analyzed using a SNP microarray. Contrary to expectations, genetic and physical distances were unrelated. This observation together with the observed lack of fixation may be explained by a large stem cell population, the de-differentiation or dormancy of stem cells, the contribution of strong purifying selection, or a combination of the previously mentioned. Our findings provide a neutral framework against which to test for module-level selection of genetic variation in corals, explore the relationship between physical and genetic distance within a colony, and apply a somatic genetic clock to colonies of Acropora palmata. This work provides necessary fundamental insights into the landscape of somatic mutations in reef-building coral, highlighting the importance of studying these mutations as they may contribute to genetic diversity and adaptability in colonial animals.

genomics↗

Seagrass arabinogalactan-proteins: Are they important for adaptation to the marine environment?

During the late cretaceous period several lineages of angiosperm plants transitioned from land to the sea by successfully adapting to life in salt water, forming the polyphyletic group of seagrasses. Today, four seagrass families inhabit coastal systems and are deeply intertwined with health and welfare of these ecosystems. Adaptation to the ocean environment included changes in the composition of plant cell walls and associated glycoproteins. We have asked the question whether or not there is a convergent and similar arabinogalactan-protein glycan repertoire in all seagrasses, given initial findings of arabinogalactan-proteins with unique features in the well-studied eelgrass, Zostera marina. We isolated and characterized arabinogalactan-proteins from seven species covering the four major seagrass families using carbohydrate analysis and glycan immunoassays, along with a bioinformatic search for relevant gene pathways in newly published seagrass genomes and transcriptomes. Glycan parts of all seagrass arabinogalactan-proteins shared a high proportion of 1,4-linked glucuronic acids and terminal 4-O-methyl glucuronic acid residues. Trait-based dendrograms generated to inform phylogenetic-relatedness showed there was no phylogenetic signal among seagrass families and arabinogalactan-protein features. Transcriptomic datasets from Cymodocea nodosa and Thalassia hemprichii growing under hypersaline conditions showed an upregulation of enzymes involved in 4O-methylation and glucuronic acid transfer. We therefore conclude that environmental factors, especially salinity with higher monovalent ion concentration, influence seagrass arabinogalactan-proteins structure more intensely than phylogenetic history.

plant biology↗

Genomic Evidence of Fisheries Induced Evolution in Eastern Baltic cod

Humans have become one of the greatest evolutionary forces, and their perturbations are expected to elicit strong evolutionary responses. Accordingly, during (size) selective overharvesting of wild populations, marked phenotypic changes have been documented, while the evolutionary basis is often unresolved. Time-series collections combined with genomic tools present unique opportunities to study how evolutionary changes are manifested at the genome-wide level. Here, we take advantage of a unique temporal dataset from the overexploited Eastern Baltic cod (Gadus morhua) population that exhibited a 48% decrease in asymptotic body length over the last 25 years. A genome-wide association study revealed pronounced peaks of outliers linked to growth performance. The contributing loci showed signals of directional selection with significantly high autocovariance in the allele frequency and excessive intersections with regions of high Fst as well as genes relevant to growth and reproduction. Moreover, pattern of directional selection for ancestral haplotype of the well-known chromosomal inversions in Atlantic cod (on linkage group 12) was observed, while the double crossover ([~]1Mb) enharbouring the vitellogenin genes within this region showed signs of drift or balancing selection. Our results demonstrate evident response of the genome over a relatively short time frame and further underscore implications for fisheries management and conservation policy regarding the adaptive potential of marine populations.

evolutionary biology↗

The chromosome-level genome of the ctenophore Mnemiopsis leidyi A. Agassiz, 1865 reveals a unique immune gene repertoire

Ctenophora are basal marine metazoans, the sister group of all other animals. Mnemiopsis leidyi is one of the most successful invasive species worldwide with intense ecological and evolutionary research interest. Here, we generated a chromosome-level genome assembly of M. leidyi with a focus on its immune gene repertoire. The genome was 247.97 Mb, with N50 16.84 Mb, and 84.7% completeness. Its karyotype was 13 chromosomes. In this genome and that of two other ctenophores, Bolinopsis microptera and Hormiphora californensis, we detected a high number of protein domains related to potential immune receptors. Among those, proteins containing Toll/interleukin-1(TIR2) domain, NACHT domain, Scavenger Receptor Cystein-Rich (SRCR) domain, or C-type Lectin domain (CTLD) were abundant and presented unique domain architectures in M. leidyi. M. leidyi seems to lack bona fide Toll like Receptors, but it does possess a repertoire of 15 TIR2-domain containing genes. Besides, we detected a bona fide NOD-like receptor and 38 NACHT-domain containing genes. In order to verify the function of those domain containing genes, we exposed M. leidyi to the pathogen Vibrio coralliilyticus. Among the differentially expressed genes, we identified potential immune receptors, including four TIR2-domain containing genes, all of which were upregulated in response to pathogen exposure. To conclude, many common immune receptor domains, highly conserved across metazoans, are already present in Ctenophora. These domains have large expansions and unique architectures in M. leidyi, findings consistent with the basal evolutionary position of this group, but still might have conserved functions in immunity and host-microbe interaction.

genomics↗

Heteroplasmy is rare in plant mitochondria compared to plastids despite similar mutation rates

Plant cells harbor two membrane-bound organelles containing their own genetic material - plastids and mitochondria. Although the two organelles co-exist and co-evolve within the same plant cells, they differ in genome copy number, intracellular organization, and mode of inheritance. How these attributes determine the time to fixation, or conversely, loss of neutral alleles is currently unresolved. Here we show that mitochondria and plastids share the same mutation rate yet plastid alleles remain in a heteroplasmic state significantly longer compared to mitochondrial alleles. By analysing genetic variants across populations of the marine flowering plant Zostera marina and simulating organelle allele dynamics, we examine the determinants of allele segregation and fixation time. Our results suggest that bottleneck on the cell population, e.g., during branching and seeding, and stratification of the meristematic tissue, are important determinants of mitochondrial allele dynamics. Furthermore, we suggest that the prolonged plastid allele dynamics are due to a yet unknown active plastid partition mechanism. The dissimilarity between plastid and mitochondrial novel allele fixation at different levels of organization may figure into differences in adaptation processes. Our study uncovers fundamental principles of organelle population genetics that are essential for further investigations of long-term evolution and molecular dating of divergence events.

bioinformatics↗

Precise age estimation in clonal species using a somatic genetic clock

Age and longevity are key parameters for demography and life-history evolution of organisms. In clonal species, a widespread life history among animals, plants, algae and fungi, the sexually produced offspring (the genet) grows indeterminately by producing iterative modules, or ramets. The age of large genets often remains elusive, while estimates based on their spatial extent as proxy for age are unreliable. Here, we present a method for age estimation using a molecular clock based on the accumulation of fixed somatic genetic variation (SoGV) that segregates among ramets of the same genet. Using a stochastic model of a generic clonal organism, we demonstrate that the accumulation of fixed SoGV via somatic genetic drift will approach linearity after a short lag phase, and is determined by the mitotic mutation rate, without direct dependence on asexual generation time. The lag phase decreased with lower stem cell population size (N), number of founder cells for the formation of new modules (N0), and the ratio of symmetric vs. asymmetric stem cell divisions. We apply the somatic genetic clock to the clonal plant model Zostera marina (eelgrass) and show that linearity is approached within a few years. Taking advantage of two long-term cultivation experiments for Z. marina (4 and 17 years respectively) as calibration points, we find genet ages up to 1,403 years in a global data set of 20 eelgrass populations. The somatic genetic clock is applicable to any multicellular clonal species where a small number of founder cells are recruited to form new ramets, opening novel research avenues to study longevity and hence, demography and population dynamics of clonal species.

evolutionary biology↗

Worldwide population genomics reveal long-term stability of the mitochondrial chromosome composition in a keystone marine plant

Mitochondrial genomes (mitogenomes) of flowering plants are comprised of multiple chromosomes. Their copy number and composition can be dynamic within and among individual plants due to uneven replication of the chromosomes and homologous recombination. Nonetheless, despite their functional importance, the level of mitogenome conservation within species remains understudied. Whether the ontogenetic variation translates to evolution of mitogenome composition over generations is currently unknown. Here we show that the mitochondrial chromosome composition of the seagrass Zostera marina is conserved among worldwide populations that diverged ca 350,000 years ago. Using long-read sequencing we characterized the Z. marina mitochondrial genome and inferred the repertoire of recombination-induced configurations of its eight chromosomes. To characterize the chromosome composition worldwide and study its evolution we examined the mitogenome in Z. marina meristematic region sampled in 16 populations from the Pacific and Atlantic oceans. Our results reveal a striking similarity in the chromosome copy number suggesting stable equal proportions among distantly related populations and a high conservation of the mitochondrial genome within the plant germline, despite a notable variability during individual ontogenesis. Our study supplies a link between observations of dynamic mitogenomes at the level of plant individuals and long-term mitochondrial evolution. Significance statementExtensive studies on evolution of plant mitochondria in individual plants revealed great variability of the mitogenome architecture across tissues, however, data on the mitochondrion evolution at the population level is still scarce. We show that the mitochondrial genome architecture in a keystone marine plant, Zostera marina, remained conserved over ca. 350,000 years worldwide. We suggest that the extreme conservation of the Z. marina mitochondria is a manifestation of streamlined mitochondria inheritance over plant generations, e.g., via a plant germline.

genomics↗

An evolutionary epigenetic clock in plants

Molecular clocks are the basis for dating the divergence between lineages over macro-evolutionary timescales (~105-108 years). However, classical DNA-based clocks tick too slowly to inform us about the recent past. Here, we demonstrate that stochastic DNA methylation changes at a subset of cytosines in plant genomes possess a clock-like behavior. This epimutation-clock is orders of magnitude faster than DNA-based clocks and enables phylogenetic explorations on a scale of years to centuries. We show experimentally that epimutation-clocks recapitulate known topologies and branching times of intra-species phylogenetic trees in the selfing plant A. thaliana and the clonal seagrass Z. marina, which represent two major modes of plant reproduction. This discovery will open new possibilities for high-resolution temporal studies of plant biodiversity.

evolutionary biology↗

Ocean currents drive the worldwide colonization of the most widespread marine plant, eelgrass (Zostera marina)

Currents are unique drivers of oceanic phylogeography and so determine the distribution of marine coastal species, along with past glaciations and sea level changes. Here, we reconstruct the worldwide colonization history of eelgrass (Zostera marina L.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Multiple west to east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival of Z. marina in the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present since [~]208 Kya (thousand years ago). Mediterranean populations were founded [~]53 Kya while extant distributions along western and eastern Atlantic shores coincide with the end of the Last Glacial Maximum ([~]20 Kya). The recent colonization and 5-to 7-fold lower genomic diversity of Atlantic compared to the Pacific populations raises concern and opportunity about how Atlantic eelgrass might respond to rapidly warming coastal oceans.

evolutionary biology↗

Using "identity by heterozygosity (IBH)" to detect clonemates under prevalent clonal reproduction in multicellular diploids

Clonal reproduction, the formation of new individuals that are genetically nearly identical to the parent via mitosis in the absence of genetic recombination, is a very common reproductive mode across plants, fungi, and animals. Current genetic marker based methods fail to detect clonal structure when all collected samples belong to one single clone, which seems to be more common than previously thought. Here we propose a new similarity index, "Shared Heterozygosity (SH)" based on the number of genetic markers (typically SNPs, single-nucleotide polymorphisms) that are identically heterozygous among two or more genomes (i.e., NSH). Ideally NSH should be on the order of approximately >=3,000, which can be easily achieved nowadays via Restriction-site Associated DNA (RAD) sequencing or whole-genome resequencing. One should be careful when NSH is small (roughly <1,000). We analyze two large seagrass clones (Posidonia australis, Zostera marina) along with two Z. marina clones of known age (17-yrs), and show that SH can potentially extend the detection of clonemates to any pair of samples with the aid of technical replicates. Another potential application of SH is to detect possible parent-descendant pairs under selfing, because the heterozygous loci in the selfing-produced descendants represent a subset of those in the parent. Our proposed workflow takes advantage of the availability of the larger number of genetic markers in the genomic era, and fills a gap in detecting clonemates in the growing number of cases where many or all samples at a location belong to one single clone.

evolutionary biology↗

Long-term culture system for deep-sea mussels Gigantidas childressi

The simulation of deep-sea conditions in laboratories is technically challenging but necessary for experiments that aim at a deeper understanding of physiological mechanisms or host-symbiont interactions of deep-sea organisms. In a proof-of-concept study, we designed a recirculating system for long-term culture (>2 years) of deep-sea mussels Gigantidas childressi (previously Bathymodiolus childressi). Mussels were automatically (and safely) supplied with a maximum stable level of ~60 {micro}M methane in seawater using a novel methane-air mixing system. Experimental animals also received daily doses of live microalgae. Condition indices of cultured G. childressi remained high over years, and low shell thickness growth could be detected, which is indicative of positive energy budgets. Using stable isotope data, we demonstrate that G. childressi in our culture system gained energy, both, from digestion of methane oxidizing endosymbionts and from digesting particulate food (microalgae). Limitations of the system, as well as opportunities for future experimental approaches involving deep-sea mussels are discussed.

ecology↗

Lower Vibrio spp. abundances in Zostera marina leaf canopies suggest a novel ecosystem function for temperate seagrass beds

Seagrasses, a polyphyletic group of about 60 marine angiosperm species, are the foundation of diverse and functionally important marine habitats along sheltered sedimentary coasts. As a novel ecological function with high societal relevance, a role of the leaf canopy for reducing potentially harmful bacteria has recently been hypothesized. Accordingly, we tested whether or not the abundance of general bacteria and more specifically, those belonging to the genus Vibrio were reduced within temperate Zostera marina (eelgrass) meadows compared to adjacent sand flats and sampled 5 sites in the south-western Baltic Sea using SCUBA. Compared to non-vegetated area, we found an average reduction of 39% for all Vibrio and 63% for the potentially harmful V. vulnificus/cholerae subtype based on robust plate counting data on Vibrio selective agar. The underlying mechanism is currently elusive and clearly merits further study. Our results underline the critical importance of seagrasses in maintaining shallow water ecosystem functioning including water quality and provide further motivation for their protection and restoration.

ecology↗

Eco-evolutionary interaction in competing phytoplankton: genotype sorting likely explains dominance shift and species responses to CO2

How ecological and evolutionary processes interact and together determine species and community responses to climate change is poorly understood. We studied long-term dynamics (over approximately 200 asexual generations) in two phytoplankton species, a coccolithophore (Emiliania huxleyi) and a diatom (Chaetoceros affinis), to increased CO2 growing alone or competing with one another in co-occurrence. To allow for rapid evolutionary responses, the experiment started with a standing genetic variation of nine genotypes in each of the species. Under co-occurrence of both species, we observed a dominance shift from C. affinis to E. huxleyi after about 120 generations in both CO2 treatments, but more pronounced under high CO2. Associated with this shift, we only found weak adaptation to high CO2 in the diatom and none in the coccolithophore in terms of species growth rates. In addition, no adaptation to interspecific competition could be observed by comparing the single to the two-species treatments in reciprocal assays, regardless of the CO2 treatment. Nevertheless, highly reproducible genotype sorting left only one genotype remaining for each of the species among all treatments. This strong evolutionary selection coincided with the dominance shift from C. affinis to E. huxleyi. Since all other conditions were kept constant over time, the most parsimonious explanation for the dominance shift is that the strong evolutionary selection potentially altered competitive ability of the two species. Thus, here observed changes in the simplest possible two-species phytoplankton "community" demonstrated that eco-evolutionary interactions can be critical for predicting community responses to climate change in rapidly dividing organisms such as phytoplankton.

evolutionary biology↗

Somatic genetic drift and multi-level selection in modular species

Cells in multicellular organisms are genetically heterogeneous owing to somatic mutations. The accumulation of somatic genetic variation in species undergoing asexual (or clonal) reproduction (termed modular species) may lead to phenotypic heterogeneity among modules. However, abundance and dynamics of somatic genetic variation under clonal growth, a widespread life history in nature, remain poorly understood. Here we show that branching events in a seagrass clone or genet leads to population bottlenecks at the cellular level and hence the evolution of genetically differentiated modules. Studying inter-module somatic genetic variation, we uncovered thousands of SNPs that segregated among modules. The strength of purifying selection on mosaic genetic variation was greater at the intra-module comparing with the inter-module level. Our study provides evidence for the operation of selection at multiple levels, of cell population and modules. Somatic genetic drift leads to the emergence of genetically unique modules; hence, modules in long-lived clonal species constitute an appropriate elementary level of selection and individuality.

evolutionary biology↗

Host-microbe interactions in the chemosynthetic Riftia pachyptila symbiosis

The deep-sea tubeworm Riftia pachyptila lacks a digestive system, but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which enabled comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. We demonstrate that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion, and substrate transfer to the symbiont by abundant host proteins. Our analysis further suggests that Riftia maintains its symbiont by protecting the bacteria from oxidative damage, while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis.

systems biology↗

Evaluating the quorum quenching potential of bacteria associated to Aurelia aurita and Mnemiopsis leidyi

The associated microbiota of marine invertebrates plays an important role to the host in relation to fitness, health and homeostasis of the metaorganism. As one key chemically-mediated interaction, Quorum sensing (QS) and interference with QS among colonizing bacteria ultimately affects the establishment and dynamics of the microbial community on the host. Aiming to address interspecies competition of cultivable microbes associated to merging model species of the basal animal phyla Cnidaria (Aurelia aurita) and Ctenophora (Mnemiopsis leidyi) as well as to evaluate their potential to shape the associated community by interfering with QS, we performed a classical isolation approach. Overall, 84 bacteria were isolated from A. aurita medusae and polyps, 64 bacteria from M. leidyi, and 83 bacteria from the ambient seawater, followed by taxonomically classification by full length 16S rRNA gene analysis. The results show that the moon jellyfish A. aurita and the comb jelly M. leidyi harbor a cultivable core microbiota consisting of typical marine and ubiquitously found bacteria (e.g. Chryseobacter, Microbacterium, Micrococcus, Olleya, Phaeobacter, Pseudoalteromonas, Pseudomonas, Rhodococcus, Shewanella, Staphylococcus, and Vibrio) which can also be found in the ambient seawater. However, several bacteria were restricted to one host (e.g. for A. aurita: Bacillus, Glaciecola, Ruegeria, Luteococcus; for M. leidyi: Acinetobacter, Aeromonas, Colwellia, Exiguobacterium, Marinomonas, Pseudoclavibacter, Psychrobacter, Sagittula, Thalassomonas) suggesting host-specific microbial community patterns. Evaluating QQ activities, out of 231 isolates, 121 showed QS-interfering activity. They mainly interfered with the acyl homoserine lactone (AHL) based communication, whereas 21 showed simultaneous quorum quenching activities against AHL and autoinducer-2. Overall, this study provides insights into the cultivable part of the microbiota associated to two environmentally important marine non-model organisms and discloses their potential in synthesizing QS interfering compounds, potentially important in shaping a healthy and resilient microbiota.

microbiology↗