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Monaghan, M. T.

Publications and source records attributed to Monaghan, M. T..

16 recordsLinked to original sources

Warming increases richness and shapes assemblages of eukaryotic parasitic plankton

BackgroundAnthropogenic activities have led to a global rise in water temperatures, prompting increased interest in how warming affects infectious disease ecology. While most studies have focused on individual host-parasite systems, there is a gap in understanding the impact of warming on multi-host, multi-parasite assemblages in natural ecosystems. To address this gap, we investigated freshwater eukaryotic parasite communities in ten natural lakes near Konin, Poland: five artificially heated and five non-heated "control" lakes. Since 1958, the heated lakes have experienced a mean annual temperature increase of 2 {degrees}C due to hot water discharge from two adjacent power plants. We collected seasonal environmental DNA (eDNA) samples from surface waters over a two-year period and applied targeted metabarcoding to compare the richness and distribution of eukaryotic parasites across lake types, with a focus on protists and fungi. ResultsUsing literature searches and sequence metadata from GenBank, we identified putative parasites which included Alveolates, Stramenopiles, basal Fungi and Ichthyosporeans, as well as their associated hosts. Heated lakes harboured distinct parasite assemblages, with higher richness of chytrids and aphelids, suggesting thermal preferences among certain freshwater microeukaryotic parasites. Other groups exhibited clear seasonal trends, with richness of oomycetes peaking in spring and summer, and that of Cryptomycota in winter and autumn. A general linear model revealed a marginally positive correlation between chytrid parasite richness and richness of their green algal, diatom, and dinoflagellate hosts. Post-hoc analyses indicated that heated lakes exhibited greater seasonal variation in chytrid parasite richness and a stronger correlation between host and parasite richness than control lakes. ConclusionThese findings demonstrate that warming can induce strong shifts in the richness and assemblages of freshwater microeukaryotic parasites. Using chytrids as a focal group, we additionally demonstrate that warming may amplify seasonal variation in parasite richness and strengthen host-parasite richness relationships.

ecology↗

The haplotype-resolved Prymnesium parvum (type B) microalga genome reveals the genetic basis of its fish-killing toxins

The catastrophic loss of aquatic life in the Central European Oder River in 2022, caused by a toxic bloom of the haptophyte microalga Prymnesium parvum (in a wide sense, s.l.), underscores the need to improve our understanding of the genomic basis of the toxin. Previous morphological, phylogenetic, and genomic studies have revealed cryptic diversity within P. parvum s.l. and uncovered three clade-specific (types A, B, C) prymnesin toxins. Here, we used state-of-the-art long-read sequencing and assembled the first haplotype-resolved diploid genome of a P. parvum type B, the strain responsible for the Oder disaster. Comparative analyses with type A genomes uncovered a genome-size expansion driven by repetitive elements in type B. We also found conserved chromosomal synteny but divergent evolution in several polyketide synthase (PKS) genes, which are known to underlie toxin production in combination with environmental cues. We identified a specific, approximately 20 kilobase pair comprising deletion in the largest PKS gene of type B that we link to differences of the chemical structure of types A and B prymnesins. Electron-microscopy and flow cytometry confirmed diploidy in the Oder River strain and differences to closely related strains in morphology and ploidy. Our results provide unprecedented resolution of strain diversity in P. parvum and a better understanding of the genomic basis of toxin variability in haptophytes. The reference-quality genome will help to understand changes to microbial diversity in the face of increasing environmental pressures, and provides a basis for strain-level monitoring of invasive Prymnesium in the future.

genomics↗

Rapid growth and the evolution of complete metamorphosis in insects

More than 60% of all animal species are insects that undergo complete metamorphosis. The key innovation of these holometabolous insects is a pupal stage between the larva and adult when most structures are completely rebuilt. Why this extreme lifestyle evolved is unclear. Here we test the hypothesis that a trade-off between growth and differentiation explains the evolution of this novelty. Using a comparative approach, we find that holometabolous insects grow much faster than hemimetabolous insects. Using a theoretical model, we then show how holometaboly evolves under a growth-differentiation trade-off and identify conditions under which such temporal decoupling of growth and differentiation is favored. Our work supports the notion that the holometabolous life history evolved to remove developmental constraints on fast growth, primarily under high mortality.

evolutionary biology↗

Phylogenomics including new sequence data of phytoplankton-infecting chytrids reveals multiple independent lifestyle transitions across the phylum

Parasitism is the most common lifestyle on Earth and has emerged many times independently across the eukaryotic tree of life. It is frequently found among chytrids (Chytridiomycota), which are early-branching unicellular fungi that feed osmotrophically via rhizoids as saprotrophs or parasites. Chytrids are abundant in most aquatic and terrestrial environments and fulfil important ecosystem functions. As parasites, they can have significant impacts on host populations. They cause global amphibian declines and influence the Earths carbon cycle by terminating algal blooms. To date, the evolution of parasitism within the chytrid phylum remains unclear due to the low phylogenetic resolution of rRNA genes for the early diversification of fungi, and because few parasitic lineages have been cultured and genomic data for parasites is scarce. Here, we combine transcriptomics, culture-independent single-cell genomics and a phylogenomic approach to overcome these limitations. We newly sequenced 29 parasitic taxa and combined these with existing data to provide a robust backbone topology for the diversification of Chytridiomycota. Our analyses reveal multiple independent lifestyle transitions between parasitism and saprotrophy among chytrids, multiple host shifts by parasites, and suggest that the chytrid last common ancestor was a parasite of phytoplankton.

evolutionary biology↗

Non-destructive DNA metabarcoding of arthropods using collection medium from passive traps

BackgroundBroad-scale monitoring of arthropods is often carried out with passive traps (e.g. Malaise traps) that can collect thousands of specimens per sample. The identification of individual specimens requires time and taxonomic expertise, limiting the geographical and temporal scale of research and monitoring studies. DNA metabarcoding of bulk-sample homogenates is faster and has been found to be efficient and reliable, but is destructive and prevents a posteriori validation of species occurrences and/or relative abundances. Non-destructive DNA metabarcoding from the collection medium has been applied in a limited number of studies, but further tests of efficiency are required in a broader range of circumstances to assess the consistency of the method. MethodsWe quantified the detection rate of arthropod species when applying non-destructive DNA metabarcoding with a short (127-bp) fragment of mitochondrial COI on two types of passive traps and collection media: 1) water with monopropylene glycol (H2O-MPG) used in window-flight traps (WFT, 53 in total); 2) ethanol with monopropylene glycol (EtOH-MPG) used in Malaise traps (MT, 27 in total). We then compared our results with those obtained for the same samples using morphological identification (for WFTs) or destructive metabarcoding of bulk homogenate (for MTs). This comparison was applied as part of a larger study of arthropod species richness in silver fir (Abies alba) stands across a range of climate-induced tree dieback levels and forest management strategies. ResultsOf the 53 H2O-MPG samples from WFTs, 16 produced no metabarcoding results, while the remaining 37 samples yielded 77 arthropod MOTUs in total. None of those MOTUs were shared species with the 389 morphological taxa (343 of which were Coleoptera) obtained from the same traps. Metabarcoding of 26 EtOH-MPG samples from MTs detected more arthropod MOTUs (233) and insect orders (11) than destructive metabarcoding of homogenate (146 MOTUs, 8 orders). Arachnida and Collembola were more diverse in EtOH-MPG samples, but Hymenoptera, Coleoptera and Lepidoptera were less represented than in homogenate. Overall, MOTU richness per trap similar for EtOH-MPG (21.81 MOTUs) than for homogenate (32.4 MOTUs). Arthropod communities from EtOH-MPG and homogenate metabarcoding were relatively distinct, with 162 MOTUs (53%) unique to the collection medium and only 71 MOTUs (23%) present in both treatments. Finally, collection medium did not reveal any significant changes in arthropod richness along a disturbance gradient in silver fir forests. We conclude that DNA metabarcoding of collection medium can be used to complement homogenate metabarcoding in inventories to favour the detection of soft-bodied arthropods like spiders.

molecular biology↗

Phylogenomics unravels the early diversification of fungi

Phylogenomic analyses have boosted our understanding of the evolutionary trajectories of all living forms by providing continuous improvements to the tree of life1-5. Within this tree, fungi represent an ancient eukaryote group6, having diverged from the animals [~]1.35 billion years ago7. Estimates of the number of extant species range between 1.5 and 3.8 million8,9. Recent reclassifications and the discovery of the deep-branching Sanchytriomycota lineage10 have brought the number of proposed phyla to 2011; 21 if the Microsporidia are included12-14. Uncovering how the diverse and globally distributed fungi are related to each other is fundamental for understanding how their lifestyles, morphologies, and metabolic capacities evolved. To date, many of the proposed relationships among the phyla remain controversial and no phylogenomic study has examined the entire fungal tree using a taxonomically comprehensive data set and suitable models of evolution. We assembled and curated a 299-protein data set with a taxon sampling broad enough to encompass all recognised fungal diversity with available data, but selective enough to run computationally intensive analyses using best-fitting models. Using a range of reconstruction methods, we were able to resolve many contested nodes, such as a sister-relationship of Chytridiomyceta to all other non-Opisthosporidia fungi (with Chytridiomycota being sister to Monoblepharomycota + Neocallimastigomycota), a branching of Blastocladiomycota + Sanchytriomycota after the Chytridiomyceta but before other non-Opisthosporidia fungi, and a branching of Glomeromycota as sister to the Dikarya. Our most up-to-date fungal tree of life will serve as a springboard for future investigations on the evolution of fungi.

evolutionary biology↗

Climate-induced forest dieback drives compositional change in insect communities that is concentrated amongst rare species

Marked decline in insect species richness, abundance and biomass have recently been quantified in Europe. We metabarcoded 224 Malaise-trap samples to investigate whether drought-induced forest dieback and subsequent salvage logging have an impact on flying insects (ca. 3000 insect species) in silver fir Pyrenean forests. We found no evidence that climate-induced forest dieback impacted species richness of flying insects but revealed compositional turnover patterns consistent with those seen during natural forest succession, given that the key covariates explaining compositional variation were canopy openness versus microhabitat diversity and deadwood amount at local and landscape scales, respectively. Importantly, most change was driven by rare species. In contrast, observed levels of salvage logging did not explain change in species richness or composition. Hence, although forest dieback appears to cause changes in species assemblages mimicking natural forest succession, it also increases the risk of catastrophic loss of rare species through homogenization of environmental conditions.

ecology↗

Climate, latitude, and land cover predict flying insect biomass across a German malaise trap network

O_LIAmong the many concerns for biodiversity in the Anthropocene, recent reports of flying insect loss are particularly alarming, given their importance as pollinators and as a food source for many predators. Few insect monitoring programs cover large spatial scales required to provide more generalizable estimates of insect responses to global change drivers. C_LIO_LIWe ask how climate and surrounding habitat affect flying insect biomass and day of peak biomass using data from the first year of a new standardized distributed monitoring network at 84 locations across Germany comprising spatial gradient of land-cover types from protected to urban areas. C_LIO_LIFlying insect biomass increased linearly with monthly temperature across Germany. However, the effect of temperature on flying insect biomass flipped to negative in the hot months of June and July when local temperatures most exceeded long-term averages. C_LIO_LILand-cover explained little variation in insect biomass, but biomass was lowest in forested sites. Grasslands, pastures and orchards harbored the highest insect biomass. The date of peak biomass was primarily driven by surrounding land-cover type, with grasslands especially having earlier insect biomass phenologies. C_LIO_LIStandardized, large-scale monitoring is pivotal to uncover underlying processes of insect decline and to develop climate-adapted strategies to promote insect diversity. In a temperate climate region, we find that the benefits of temperature on flying insect biomass diminish in a German summer at locations where temperatures most exceeded long-term averages. These results highlighting the importance of local adaptation in climate change-driven impacts on insect communities. C_LI

ecology↗

Identification of enzymes for lignocellulose degradation in the genome and transcriptome of the aquatic hyphomycete Clavariopsis aquatica.

Fungi are ecologically important decomposers of lignocellulose. Basidiomycetes use peroxidases, laccases, and enzymes of the cytochrome P450 superfamily for cometabolic lignin degradation in order to access cellulose and hemicellulose as carbon sources. Limited lignin modification capabilities have also been reported for some terrestrial ascomycetes. Here we newly sequenced the genome of an exclusively aquatic ascomycete, Clavariopsis aquatica, documented the presence of genes for the modification of lignocellulose and its constituents, and compared differential gene expression between C. aquatica cultivated on lignocellulosic and sugar-rich substrates. We identified potential peroxidases, laccases, and cytochrome P450 monooxygenases several of which were differentially expressed when experimentally grown on different substrates. Additionally, we found regulation of pathways for cellulose and hemicellulose degradation. Our results suggest that C. aquatica is able to modify lignin, detoxify aromatic lignin constituents, or both. This may facilitate the use of carbohydrate components of lignocellulose as carbon and energy sources.

ecology↗

PriSeT: Efficient De Novo Primer Discovery

MotivationDNA metabarcoding is a commonly applied technique used to infer the species composition of environmental samples. These samples can comprise hundreds of organisms that can be closely or very distantly related in the taxonomic tree of life. DNA metabarcoding combines polymerase chain reaction (PCR) and next-generation sequencing (NGS), whereby a short, homologous sequence of DNA is amplified and sequenced from all members of the community. Sequences are then taxonomically identified based on their match to a reference database. Ideally, each species of interest would have a unique DNA barcode. This short, variable sequence needs to be flanked by relatively conserved regions that can be used as primer binding sites. Appropriate PCR primer pairs would match to a broad evolutionary range of taxa, such that we only need a few to achieve high taxonomic coverage. At the same time however, the DNA barcodes between primer pairs should be different to allow us to distinguish between species to improve resolution. This poses an interesting optimization problem. More specifically: Given a set of references [R] = {R1, R2, ..., Rm}, the problem is to find a primer set P balancing both: high taxonomic coverage and high resolution. This goal can be captured by filtering for frequent primers and ranking by coverage or variation, i.e. the number of unique barcodes. Here we present the software PriSeT, an offline primer discovery tool that is capable of processing large libraries and is robust against mislabeled or low quality references. It tackles the computationally expensive steps with linear runtime filters and efficient encodings. ResultsWe first evaluated PriSeT on references (mostly 18S rRNA genes) from 19 clades covering eukaryotic organisms that are typical for freshwater plankton samples. PriSeT recovered several published primer sets as well as additional, more chemically suitable primer sets. For these new sets, we compared frequency, taxon coverage, and amplicon variation with published primer sets. For 11 clades we found de novo primer pairs that cover more taxa than the published ones, and for six clades de novo primers resulted in greater sequence (i.e., DNA barcode) variation. We also applied PriSeT to 19 SARS-CoV-2 genomes and computed 114 new primer pairs with the additional constraint that the sequences have no co-occurrences in other taxa. These primer sets would be suitable for empirical testing. Availabilityhttps://github.com/mariehoffmann/PriSeT Contactmarie.hoffmann@fu-berlin.de

bioinformatics↗

Comparative population genetic structure of two Ixodidae ticks (Ixodes ovatus and Haemaphysalis flava) in Niigata Prefecture, Japan

Ixodid tick species such as Ixodes ovatus and Haemaphysalis flava are essential vectors of tick-borne diseases in Japan. In this study, we investigated the population genetic structures and gene flow of I. ovatus and H. flava as affected by the tick host mobility. We hypothesized that I. ovatus and H. flava may have differences in their genetic structure due to the low mobility of small rodent hosts of I. ovatus at the immature stage in contrast to the mediated dispersal of avian hosts for immature H. flava. We collected 307 adult I. ovatus and 220 adult H. flava from 29 and 17 locations across Niigata Prefecture, Japan. We investigated the genetic structure at two mitochondrial loci (cox1, 16S rRNA gene). For I. ovatus, pairwise FST and analysis of molecular variance (AMOVA) analyses of cox1 sequences indicated significant genetic variation among populations. Both cox1 and 16S rRNA markers showed non-significant genetic variation among locations for H. flava. The Bayesian tree and haplotype network of cox1 marker for I. ovatus samples in Niigata Prefecture found 3 genetic groups wherein most haplotypes in group 2 were distributed in low altitudinal areas. When we added cox1 sequences of I. ovatus from China to the phylogenetic analysis, three genetic groups (China 1, China 2, and Niigata and Hokkaido, Japan) were formed in the tree suggesting the potential for cryptic species in the genetic group in Japan. Our results support our hypothesis and suggest that the host preference of ticks at the immature stage may influence the genetic structure and gene flow of the ticks. This information is vital in understanding the tick-host interactions in the field to better understand the tick-borne disease transmission and in designing an effective tick control program.

genetics↗

Spatial and phylogenetic structure of DNA-species of Alpine stonefly community assemblages across seven habitats

O_LIStream ecosystems are spatially heterogeneous, with many different habitat patches distributed within a small area. The influence of this heterogeneity on the biodiversity of benthic insect communities is well documented; however, studies of the role of habitat heterogeneity in species coexistence and community assembly remain limited. Here, we investigated how habitat heterogeneity influences spatial structure (beta biodiversity) and phylogenetic structure (evolutionary processes) of benthic stonefly (Plecoptera, Insecta) communities. C_LIO_LIWe sampled 20 sites along two Alpine rivers, including seven habitats in four different reaches (headwaters, meandering, bar-braided floodplain, and lowland spring-fed). We identified 21 morphological species and delineated 52 DNA-species based on sequences from mitochondrial cox1 and nuclear ITS markers. Using DNA-species, we first analysed the patterns of variation in richness, diversity, and community composition by quantifing the contribution of each of the four reaches and seven habitats to the overall DNA-species diversity using an additive partition of species diversity analysis and distance-based redundancy analysis. Using gene-tree phylogenies, we assessed whether environmental filtering led to the co-occurrence of DNA-species using a two-step analysis to find a phylogenetic signal. C_LIO_LIThe four reaches significantly contributed to DNA-species richness; with the meandering section having the highest contribution. However, we found that habitats had an effect on DNA-species diversity, where glide, riffle and, pool influenced the spatial structure of stonefly communities possibly due to a high species turnover. C_LIO_LIAmong the habitats, the pool showed significant phylogenetic clustering, suggesting high levels of evolutionary adaptation and strong habitat filtering. This community structure may be caused by long-term stability of the habitat and the similar requirements for co-occurring species. C_LIO_LIOur study shows the importance of different habitats on the spatial and phylogenetic structure of stonefly community assemblies and sheds light on the habitat-specific diversity that may help improve conservation practices. C_LI

evolutionary biology↗

Combining the 5.8S and ITS2 gene regions to improve classification of fungi

O_LIThe internal transcribed spacer (ITS) is used in DNA metabarcoding of fungi. One disadvantage of its high variability may be a failure to classify OTUs when no similar reference sequence exists. We tested whether the 5.8S region, often sequenced with ITS2 but discarded before analysis, could provide OUT classifications when ITS fails. C_LIO_LIWe used in silico evaluation to compare classification success of 5.8S and ITS from the UNITE database when reference sequences of the same species, genus, or family were removed. We then developed an automated pipeline for a combined 5.8S - ITS2 analysis and applied it to mixed environmental samples containing many lineages that are underrepresented in databases. C_LIO_LIITS was clearly superior for species-level classifications with a complete reference database, but 5.8S outperformed ITS at higher level classifications with an incomplete database. Our combined 5.8S-ITS2 pipeline classified 3x more fungal OTUs compared to ITS2 alone, particularly within Chytridiomycota (10x) and Rozellamycota (3x). C_LIO_LIMissing reference sequences led to the failure of ITS to classify many fungal OTUs at all, and to a significant underestimation of environmental fungal diversity. Using 5.8S to complement ITS classification will likely provide better estimates of diversity in lineages for which database coverage is poor. C_LI

ecology↗

Long-read DNA metabarcoding of ribosomal rRNA in the analysis of fungi from aquatic environments

DNA metabarcoding is now widely used to study prokaryotic and eukaryotic microbial diversity. Technological constraints have limited most studies to marker lengths of ca. 300-600 bp. Longer sequencing reads of several 5 thousand bp are now possible with third-generation sequencing. The increased marker lengths provide greater taxonomic resolution and enable the use of phylogenetic methods of classifcation, but longer reads may be subject to higher rates of sequencing error and chimera formation. In addition, most well-established bioinformatics tools for DNA metabarcoding were originally 10 designed for short reads and are therefore not suitable. Here we used Pacifc Biosciences circular consensus sequencing (CCS) to DNA-metabarcode environmental samples using a ca. 4,500 bp marker that included most of the eukaryote ribosomal SSU and LSU rRNA genes and the ITS spacer region. We developed a long-read analysis pipeline that reduced error rates to levels 15 comparable to short-read platforms. Validation using fungal isolates and a mock community indicated that our pipeline detected 98% of chimeras de novo i.e., even in the absence of reference sequences. We recovered 947 OTUs from water and sediment samples in a natural lake, 848 of which could be classifed to phylum, 486 to family, 397 to genus and 330 to species. By 20 allowing for the simultaneous use of three global databases (Unite, SILVA, RDP LSU), long-read DNA metabarcoding provided better taxonomic resolution than any single marker. We foresee the use of long reads enabling the cross-validation of reference sequences and the synthesis of ribosomal rRNA gene databases. The universal nature of the rRNA operon and our recovery of >100 25 non-fungal OTUs indicate that long-read DNA metabarcoding holds promise for the study of eukaryotic diversity more broadly.

ecology↗

Stress response of Chironomus riparius to changes in water temperature and oxygen concentration in a lowland stream

The increasing impairment of lotic ecosystems has promoted a growing effort into assessing their ecological status by means of biological indicators. While community-based approaches have proven valuable to assess ecosystem integrity, they mostly reflect long-term changes and might not be suitable for tracking and monitoring short-term events. Responses to rapid changes in environmental conditions have been rarely studied under natural conditions. Biomarkers offer the benefit of integrating biological responses at different time scales. Here we used a field experiment to test how the synthesis of heat shock protein 70 (HSP70) and Haemoglobin (Hb) in laboratory-reared larvae of Chironomus riparius (Diptera, Chironomidae) were influenced by short-term changes to water temperature and oxygen concentration in a lowland stream. Our aim was to determine whether HSP70 mRNA expression and Hb content could be used as an in situ \"early warning system\" for freshwater habitats undergoing environmental change. HSP70 exhibited a clear response to changes in temperature measured over a one-day period, confirming its suitability as an indicator of environmental stress. Hb concentration was related to oxygen concentration, but not to temperature. Our findings support the hypothesis that depletion in oxygen induces Hb synthesis in C. riparius larvae. Because tolerance to low oxygen is not only related to total Hb, but also to a more efficient uptake (binding to Hb, e.g. Bohr effect) and release of oxygen to the cell (Root effect), we cannot discern from our data whether increased efficiency played a role. We suggest that C. riparius is a suitable model organism for monitoring sub-lethal stress in the field and that the approach could be applied to other species as more genomic data are available for non-model organisms.

zoology↗

Mitochondrial genomes infer phylogenetic relationships among the oldest extant winged insects (Palaeoptera)

Phylogenetic relationships among the basal orders of winged insects remain unclear, in particular the relationship of the Ephemeroptera (mayflies) and the Odonata (dragonflies and damselflies) with the Neoptera. Insect evolution is thought to have followed rapid divergence in the distant past and phylogenetic reconstruction may therefore be susceptible to problems of taxon sampling, choice of outgroup, marker selection, and tree reconstruction method. Here we newly sequenced three mitochondrial genomes representing the two most diverse families of the Ephemeroptera, one of which is a basal lineage of the order. We then used an additional 90 insect mitochondrial genomes to reconstruct their phylogeny using Bayesian and maximum likelihood approaches. Bayesian analysis supported a basal Odonata hypothesis, with Ephemeroptera as sister group to the remaining insects. This was only supported when using an optimized data matrix from which rogue taxa and terminals affected by long-branch attraction were removed. None of our analyses supported a basal Ephemeroptera hypothesis or Ephemeroptera + Odonata as monophyletic clade sister to other insects (i.e., the Palaeoptera hypothesis). Our newly sequenced mitochondrial genomes of Baetis rutilocylindratus, Cloeon dipterum, and Habrophlebiodes zijinensis had a complete set of protein coding genes and a conserved orientation except for two inverted tRNAs in H. zijinensis. Increased mayfly sampling, removal of problematic taxa, and a Bayesian phylogenetic framework were needed to infer phylogenetic relationships within the three ancient insect lineages of Odonata, Ephemeroptera, and Neoptera. Pruning of rogue taxa improved the number of supported nodes in all phylogenetic trees. Our results add to previous evidence for the Odonata hypothesis and indicate that the phylogenetic resolution of the basal insects can be resolved with more data and sampling effort.

evolutionary biology↗