One tunic but more than one barcode: evolutionary insights from dynamic mitochondrial DNA in Salpa thompsoni (Tunicata: Salpida)

The DNA barcode within the mitochondrial cox1 gene is typically used to assess the identity and diversity of animals under the assumption that individuals contain a single form of this genetic marker. This study reports on a novel exception from the pelagic tunicate Salpa thompsoni Foxton. Oozoids caught off South Georgia and the Antarctic Peninsula generated barcodes consisting of a single prominent DNA sequence with some additional, subtler signals of intra-individual variation. Further investigation revealed this was due to duplicated and/or minicircular DNAs. These could not simply be explained as artefacts or nuclear copies of mitochondrial DNA, but provided evidence for heteroplasmy arising from a dynamic mitochondrial genome. Genetic variation of this sort may allow S. thompsoni to ecologically benefit from asexually driven population blooms without incurring the genetic cost of an excessive mutational load. Analysis of the prominent barcode sequence data yielded low haplotype (h < 0.61) and nucleotide (π < 0.0014) diversities, and no evidence for genetic structure between sampling locations as assessed using analysis of molecular variance. These results are consistent with the impact of population blooms and the mixing effect of Southern Ocean currents on S. thompsoni genetic diversity

Liverworts frequently form mycothalli on Spitsbergen in the High Arctic

Mycothalli, symbioses between liverworts and soil fungi, have not previously been recorded in the Arctic. Here, 13 species of leafy liverwort from west Spitsbergen in the High Arctic are examined for the symbiosis using epifluorescence microscopy and sequencing of fungal ribosomal (r)RNA genes amplified from plant tissues. Microscopy showed that intracellular hyphal coils, key indicators of the symbiosis, were frequent (>40% stem length colonized) in nine species of liverwort in the families Anastrophyllaceae, Lophoziaceae, Cephaloziellaceae, Cephaloziaceae and Scapaniaceae, with hyphae occurring frequently (>40% cells occupied) in the rhizoids of 10 species in the same families. Dark septate hyphae, apparently formed by ascomycetes, were frequent on the stems of members of the Anastrophyllaceae, Cephaloziellaceae and Cephaloziaceae, and typically those growing on acidic mine tailings. Sequencing of fungal rRNA genes showed the presence of nine distinct groups (based on a 3% cut-off for ITS sequence divergence) of the basidiomycete Serendipita in the Anastrophyllaceae and Lophoziaceae, with ordinations and correlative analyses showing the presence of the genus to be positively associated with the frequency of hyphal coils, the occurrence of which was positively associated with edaphic factors (soil δ15N value and concentrations of moisture, nitrogen, carbon and organic matter). We propose that the frequency of mycothalli in leafy liverworts on west Spitsbergen, which is an order of magnitude higher than at lower latitudes, may arise from benefits conferred by mycobionts on their hosts in the harsh environment of the High Arctic

Experimental warming increases fungal alpha diversity in an oligotrophic maritime Antarctic soil

The climate of maritime Antarctica has altered since the 1950s. However, the effects of increased temperature, precipitation and organic carbon and nitrogen availability on the fungal communities inhabiting the barren and oligotrophic fellfield soils that are widespread across the region are poorly understood. Here, we test how warming with open top chambers (OTCs), irrigation and the organic substrates glucose, glycine and tryptone soy broth (TSB) influence a fungal community inhabiting an oligotrophic maritime Antarctic fellfield soil. In contrast with studies in vegetated soils at lower latitudes, OTCs increased fungal community alpha diversity (Simpson’s index and evenness) by 102–142% in unamended soil after 5 years. Conversely, OTCs had few effects on diversity in substrate-amended soils, with their only main effects, in glycine-amended soils, being attributable to an abundance of Pseudogymnoascus. The substrates reduced alpha and beta diversity metrics by 18–63%, altered community composition and elevated soil fungal DNA concentrations by 1–2 orders of magnitude after 5 years. In glycine-amended soil, OTCs decreased DNA concentrations by 57% and increased the relative abundance of the yeast Vishniacozyma by 45-fold. The relative abundance of the yeast Gelidatrema declined by 78% in chambered soil and increased by 1.9-fold in irrigated soil. Fungal DNA concentrations were also halved by irrigation in TSB-amended soils. In support of regional- and continental-scale studies across climatic gradients, the observations indicate that soil fungal alpha diversity in maritime Antarctica will increase as the region warms, but suggest that the accumulation of organic carbon and nitrogen compounds in fellfield soils arising from expanding plant populations are likely, in time, to attenuate the positive effects of warming on diversity. Antarctica, climate warming, open top chambers (OTCs), organic carbon, organic nitrogen, soil fungal community diversity, yeastspublishedVersio

Experimental warming increases fungal alpha diversity in an oligotrophic maritime Antarctic soil

The climate of maritime Antarctica has altered since the 1950s. However, the effects of increased temperature, precipitation and organic carbon and nitrogen availability on the fungal communities inhabiting the barren and oligotrophic fellfield soils that are widespread across the region are poorly understood. Here, we test how warming with open top chambers (OTCs), irrigation and the organic substrates glucose, glycine and tryptone soy broth (TSB) influence a fungal community inhabiting an oligotrophic maritime Antarctic fellfield soil. In contrast with studies in vegetated soils at lower latitudes, OTCs increased fungal community alpha diversity (Simpson’s index and evenness) by 102–142% in unamended soil after 5 years. Conversely, OTCs had few effects on diversity in substrate-amended soils, with their only main effects, in glycine-amended soils, being attributable to an abundance of Pseudogymnoascus. The substrates reduced alpha and beta diversity metrics by 18–63%, altered community composition and elevated soil fungal DNA concentrations by 1–2 orders of magnitude after 5 years. In glycine-amended soil, OTCs decreased DNA concentrations by 57% and increased the relative abundance of the yeast Vishniacozyma by 45-fold. The relative abundance of the yeast Gelidatrema declined by 78% in chambered soil and increased by 1.9-fold in irrigated soil. Fungal DNA concentrations were also halved by irrigation in TSB-amended soils. In support of regional- and continental-scale studies across climatic gradients, the observations indicate that soil fungal alpha diversity in maritime Antarctica will increase as the region warms, but suggest that the accumulation of organic carbon and nitrogen compounds in fellfield soils arising from expanding plant populations are likely, in time, to attenuate the positive effects of warming on diversity. Antarctica, climate warming, open top chambers (OTCs), organic carbon, organic nitrogen, soil fungal community diversity, yeastspublishedVersio

Experimental warming increases fungal alpha diversity in an oligotrophic maritime Antarctic soil

The climate of maritime Antarctica has altered since the 1950s. However, the effects of increased temperature, precipitation and organic carbon and nitrogen availability on the fungal communities inhabiting the barren and oligotrophic fellfield soils that are widespread across the region are poorly understood. Here, we test how warming with open top chambers (OTCs), irrigation and the organic substrates glucose, glycine and tryptone soy broth (TSB) influence a fungal community inhabiting an oligotrophic maritime Antarctic fellfield soil. In contrast with studies in vegetated soils at lower latitudes, OTCs increased fungal community alpha diversity (Simpson’s index and evenness) by 102–142% in unamended soil after 5 years. Conversely, OTCs had few effects on diversity in substrate-amended soils, with their only main effects, in glycine-amended soils, being attributable to an abundance of Pseudogymnoascus. The substrates reduced alpha and beta diversity metrics by 18–63%, altered community composition and elevated soil fungal DNA concentrations by 1–2 orders of magnitude after 5 years. In glycine-amended soil, OTCs decreased DNA concentrations by 57% and increased the relative abundance of the yeast Vishniacozyma by 45-fold. The relative abundance of the yeast Gelidatrema declined by 78% in chambered soil and increased by 1.9-fold in irrigated soil. Fungal DNA concentrations were also halved by irrigation in TSB-amended soils. In support of regional- and continental-scale studies across climatic gradients, the observations indicate that soil fungal alpha diversity in maritime Antarctica will increase as the region warms, but suggest that the accumulation of organic carbon and nitrogen compounds in fellfield soils arising from expanding plant populations are likely, in time, to attenuate the positive effects of warming on diversity. Antarctica, climate warming, open top chambers (OTCs), organic carbon, organic nitrogen, soil fungal community diversity, yeastspublishedVersio

Inhibitory effects of climate change on the growth and extracellular enzyme activities of a widespread Antarctic soil fungus

Temperatures approaching or exceeding 20 °C have been measured during summer in polar regions at the surfaces of barren fellfield soils under cloudless skies around solar noon. However, despite the upper temperature limit for the growth of cold‐adapted microbes – which are abundant in polar soils and have pivotal roles in nutrient cycling – typically being close to this temperature, previous studies have not addressed the consequences of climate change for the metabolism of these organisms in the natural environment. Here, in a five‐year field experiment on Alexander Island in the southern maritime Antarctic, we show that the abundance of Pseudogymnoascus roseus, the most widespread decomposer fungus in maritime Antarctic fellfield soils, is reduced by 1–2 orders of magnitude when irrigated and nutrient‐amended soils are warmed to >20 °C during summer. Laboratory experiments under conditions mimicking those during midsummer in the natural environment indicated that the hyphal extension rates of P. roseus isolates and the activities of five extracellular enzymes are reduced by 54–96% at high water availability after exposure to temperatures cycling daily from 2–21 °C and 2–24 °C, relative to temperatures cycling from 2–18 °C. Given that the temperatures of surface soils at the study site already reach 19 °C during midsummer, the observations reported here suggest that, at predicted rates of warming arising from moderate greenhouse gas emissions, inhibitory effects of climate change on the metabolism of P. roseus could manifest themselves within the next few decades. Furthermore, with peak temperatures at the surfaces of fellfield soils at other maritime Antarctic locations and in High Arctic and alpine regions already exceeding 20 °C during summer, the observations suggest that climate warming has the potential to inhibit the growth of other cold‐adapted microbes, with negative effects on soils as the Earth’s climate continues to war

The “Trojan horse” strategy: Seed fungal endophyte symbiosis helps to explain the invasion success of the grass, Poa annua, in Maritime Antarctica

Aim Poa annua L. (annual bluegrass) is presently the sole invasive vascular plant species to have successfully established in Maritime Antarctica, where it poses a significant conservation threat to native plant species. However, the reasons for its success in the region have yet to be established. Here, we determined whether the invasiveness of P. annua, and its competitiveness with the native Antarctic hairgrass Deschampsia antarctica, is influenced by symbioses formed with seed fungal endophytes, and whether plants derived from seeds from four global regions differ in their performance. Locations Four regions (Maritime Antarctica, sub-Antarctica, South America and Europe). Methods Endophyte frequency was measured in P. annua seeds collected from the four regions. The germination, survival, biomass accumulation, flowering and competitiveness with D. antarctica of P. annua plants grown from endophyte-uncolonised and uncolonised seeds was determined in the laboratory. The effects of endophytes on P. annua seed germination and survival and seedling osmoprotection were also assessed in the Maritime Antarctic natural environment using locally-sourced seeds. Results Endophytes were at least twice as frequent in seeds from Maritime Antarctica than in those from other regions. A higher proportion of endophyte-colonized seeds germinated and survived than did uncolonised seeds, but only when they originated from Maritime Antarctica. Seed endophytes increased the competitiveness of P. annua with D. antarctica, but only for plants grown from Maritime Antarctic seeds. In the field, endophyte-colonized seeds from Maritime Antarctica germinated and survived more frequently than uncolonised seeds, and osmoprotection was higher in seedlings grown from colonized seed. Main Conclusions The findings indicate beneficial effects of seed endophytes on invasion-related traits of P. annua, such as survival, germination success and flowering. Together with vegetative and reproductive traits facilitating the colonization process, the seed-fungal endophyte symbiosis can be invoked as an important factor explaining the invasiveness of P. annua in Maritime Antarctica

Multiple late-Pleistocene colonisation events of the Antarctic pearlwort Colobanthus quitensis (Caryophyllaceae) reveal the recent arrival of native Antarctic vascular flora

Aim: Antarctica's remote and extreme terrestrial environments are inhabited by only two species of native vascular plants. We assessed genetic connectivity amongst Antarctic and South American populations of one of these species, Colobanthus quitensis, to determine its origin and age in Antarctica. Location: Maritime Antarctic, sub‐Antarctic islands, South America. Taxon: Antarctic pearlwort Colobanthus quitensis (Caryophyllaceae). Methods: Four chloroplast markers and one nuclear marker were sequenced from 270 samples from a latitudinal transect spanning 21–68° S. Phylogeographic, population genetic and molecular dating analyses were used to assess the demographic history of C. quitensis and the age of the species in Antarctica. Results: Maritime Antarctic populations consisted of two different haplotype clusters, occupying the northern and southern Maritime Antarctic. Molecular dating analyses suggested C. quitensis to be a young (<1 Ma) species, with contemporary population structure derived since the late‐Pleistocene. Main conclusions: The Maritime Antarctic populations likely derived from two independent, late‐Pleistocene dispersal events. Both clusters shared haplotypes with sub‐Antarctic South Georgia, suggesting higher connectivity across the Southern Ocean than previously thought. The overall findings of multiple colonization events by a vascular plant species to Antarctica, and the recent timing of these events, are of significance with respect to future colonizations of the Antarctic Peninsula by vascular plants, particularly with predicted increases in ice‐free land in this area. This study fills a significant gap in our knowledge of the age of the contemporary Antarctic terrestrial biota. Adding to previous inferences on the other Antarctic vascular plant species (the grass Deschampsia antarctica), we suggest that both angiosperm species are likely to have arrived on a recent (late‐Pleistocene) time‐scale. While most major groups of Antarctic terrestrial biota include examples of much longer‐term Antarctic persistence, the vascular flora stands out as the first identified terrestrial group that appears to be of recent origin

Data from: The molecular evolution of spiggin nesting glue in sticklebacks

Gene duplication and subsequent divergence can lead to the evolution of new functions and lineage-specific traits. In sticklebacks, the successive duplication of a mucin gene (MUC19) into a tandemly arrayed, multigene family has enabled the production of copious amounts of ‘spiggin’, a secreted adhesive protein essential for nest construction. Here, we examine divergence between spiggin genes among three-spined sticklebacks (Gasterosteus aculeatus) from ancestral marine and derived freshwater populations, and propose underpinning gene duplication mechanisms. Sanger sequencing revealed substantial diversity among spiggin transcripts, including alternatively spliced variants and interchromosomal spiggin chimeric genes. Comparative analysis of the sequenced transcripts and all other spiggin genes in the public domain support the presence of three main spiggin lineages (spiggin A, spiggin B and spiggin C) with further subdivisions within spiggin B (B1, B2) and spiggin C (C1, C2). Spiggin A had diverged least from the ancestral MUC19, while the spiggin C duplicates had diversified most substantially. In silico translations of the spiggin gene open reading frames predicted that spiggins A and B are secreted as long mucin-like polymers, while spiggins C1 and C2 are secreted as short monomers, with putative antimicrobial properties. We propose that diversification of duplicated spiggin genes has facilitated local adaptation of spiggin to a range of aquatic habitats

Data from: The molecular evolution of spiggin nesting glue in sticklebacks

Gene duplication and subsequent divergence can lead to the evolution of new functions and lineage-specific traits. In sticklebacks, the successive duplication of a mucin gene (MUC19) into a tandemly arrayed, multigene family has enabled the production of copious amounts of ‘spiggin’, a secreted adhesive protein essential for nest construction. Here, we examine divergence between spiggin genes among three-spined sticklebacks (Gasterosteus aculeatus) from ancestral marine and derived freshwater populations, and propose underpinning gene duplication mechanisms. Sanger sequencing revealed substantial diversity among spiggin transcripts, including alternatively spliced variants and interchromosomal spiggin chimeric genes. Comparative analysis of the sequenced transcripts and all other spiggin genes in the public domain support the presence of three main spiggin lineages (spiggin A, spiggin B and spiggin C) with further subdivisions within spiggin B (B1, B2) and spiggin C (C1, C2). Spiggin A had diverged least from the ancestral MUC19, while the spiggin C duplicates had diversified most substantially. In silico translations of the spiggin gene open reading frames predicted that spiggins A and B are secreted as long mucin-like polymers, while spiggins C1 and C2 are secreted as short monomers, with putative antimicrobial properties. We propose that diversification of duplicated spiggin genes has facilitated local adaptation of spiggin to a range of aquatic habitats