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Methane-cycling is becoming more important in high-latitude ecosystems as global warming makes permafrost organic carbon increasingly available. We explored 387 samples from three high-latitudes regions (Siberia, Alaska and Patagonia) focusing on mineral/organic soils (wetlands, peatlands, forest), lake/pond sediment and water. Physicochemical, climatic and geographic variables were integrated with 16S rDNA amplicon sequences to determine the structure of the overall microbial communities and of specific methanogenic and methanotrophic guilds. Physicochemistry (especially pH) explained the largest proportion of variation in guild composition, confirming species sorting (i.e., environmental filtering) as a key mechanism in microbial assembly. Geographic distance impacted more strongly beta diversity for (i) methanogens and methanotrophs than the overall prokaryotes and, (ii) the sediment habitat, suggesting that dispersal limitation contributed to shape the communities of methane-cycling microorganisms. Bioindicator taxa characterising different ecological niches (i.e., specific combinations of geographic, climatic and physicochemical variables) were identified, highlighting the importance of Methanoregula as generalist methanogens. Methylocystis and Methylocapsa were key methanotrophs in low pH niches while Methylobacter and Methylomonadaceae in neutral environments. This work gives insight into the present and projected distribution of methane-cycling microbes at high latitudes under climate change predictions, which is crucial for constraining their impact on greenhouse gas budgets.
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Euryarchaeota , Microbiota , Microbiota/genética , Euryarchaeota/genética , Áreas Alagadas , Solo/química , MetanoRESUMO
Ancestral adaptations to tropical-like climates drive most multicellular biogeography and macroecology. Observational studies suggest that this niche conservatism could also be shaping unicellular biogeography and macroecology, although evidence is limited to Acidobacteria and testate amoebae. We tracked the phylogenetic signal of this niche conservatism in far related and functionally contrasted groups of common soil protists (Bacillariophyta, Cercomonadida, Ciliophora, Euglyphida and Kinetoplastida) along a humid but increasingly cold elevational gradient in Switzerland. Protist diversity decreased, and the size of the geographic ranges of taxa increased with elevation and associated decreasing temperature (climate), which is consistent with a macroecological pattern known as the Rapoport effect. Bacillariophyta exhibited phylogenetically overdispersed communities assembled by competitive exclusion of closely related taxa with shared (conserved) niches. By contrast, Cercomonadida, Ciliophora, Euglyphida and Kinetoplastida exhibited phylogenetically clustered communities assembled by habitat filtering, revealing the coexistence of closely related taxa with shared (conserved) adaptations to cope with the humid but temperate to cold climate of the study site. Phylobetadiversity revealed that soil protists exhibit a strong phylogenetic turnover among elevational sites, suggesting that most taxa have evolutionary constraints that prevent them from colonizing the colder and higher sites of the elevation gradient. Our results suggest that evolutionary constraints determine how soil protists colonize climates departing from warm and humid conditions. We posit that these evolutionary constraints are linked to an ancestral adaptation to tropical-like climates, which limits their survival in exceedingly cold sites. This niche conservatism possibly drives their biogeography and macroecology along latitudinal and altitudinal climatic gradients.
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Cilióforos , Solo , Biodiversidade , Cilióforos/genética , Ecossistema , FilogeniaRESUMO
Assessing the degree to which climate explains the spatial distributions of different taxonomic and functional groups is essential for anticipating the effects of climate change on ecosystems. Most effort so far has focused on above-ground organisms, which offer only a partial view on the response of biodiversity to environmental gradients. Here including both above- and below-ground organisms, we quantified the degree of topoclimatic control on the occurrence patterns of >1,500 taxa and phylotypes along a c. 3,000 m elevation gradient, by fitting species distribution models. Higher model performances for animals and plants than for soil microbes (fungi, bacteria and protists) suggest that the direct influence of topoclimate is stronger on above-ground species than on below-ground microorganisms. Accordingly, direct climate change effects are predicted to be stronger for above-ground than for below-ground taxa, whereas factors expressing local soil microclimate and geochemistry are likely more important to explain and forecast the occurrence patterns of soil microbiota. Detailed mapping and future scenarios of soil microclimate and microhabitats, together with comparative studies of interacting and ecologically dependent above- and below-ground biota, are thus needed to understand and realistically forecast the future distribution of ecosystems.
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Biodiversidade , Ecossistema , Animais , Mudança Climática , Microclima , Solo , Microbiologia do SoloRESUMO
Hanging is one of the most common methods of suicide, and, although it is known that decomposition and patterns of insect fauna colonization of hanging cadavers differ from those of cadavers decomposing on the ground, these differences have only been sparsely studied in Europe so far. We studied the decomposition and insect colonization patterns of ten pig (Sus scrofa domestica) carcasses in a spruce forest near Neuchâtel, Switzerland, over a 32-day period in summer 2013 (July 1st - August 2nd). Five pig carcasses were suspended horizontally in metal cages one meter above the ground and five carcasses were placed directly on the ground. The species occurrence and abundance of Coleoptera and Diptera recovered from passive pitfall traps and collected manually on the carcasses were recorded. Indicator species of decomposition stages and suspended vs. ground cadavers were identified by Indicator Value (IndVal) analysis. The ground carcasses decomposed significantly faster than the suspended carcasses. Coleoptera and Diptera communities differed significantly over time, between treatment, and the treatment effect varied over time. Diptera were evenly distributed among the two treatments. Coleoptera were more abundant and less differentiated on the ground carcasses and represent better indicators of cadavers decomposing on the soil as well as decomposition stages. Our results suggest possible applications such as evaluating if a hanged cadaver has been dropped to the ground, or inversely if a cadaver first lying on the soil has later been hung to fake a suicide. However differences among studies suggest possible effects of meso-climate determined by habitat which should be explored further.
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Besouros , Dípteros , Comportamento Alimentar , Mudanças Depois da Morte , Solo , Animais , Entomologia , Patologia Legal/métodos , Modelos Animais , Suínos , SuíçaRESUMO
The community composition of any group of organisms should theoretically be determined by a combination of assembly processes including resource partitioning, competition, environmental filtering, and phylogenetic legacy. Environmental DNA studies have revealed a huge diversity of protists in all environments, raising questions about the ecological significance of such diversity and the degree to which they obey to the same rules as macroscopic organisms. The fast-growing cultivable protist species on which hypotheses are usually experimentally tested represent only a minority of the protist diversity. Addressing these questions for the lesser known majority can only be inferred through observational studies. We conducted an environmental DNA survey of the genus Nebela, a group of closely related testate (shelled) amoeba species, in different habitats within Sphagnum-dominated peatlands. Identification based on the mitochondrial cytochrome c oxidase 1 gene, allowed species-level resolution as well as phylogenetic reconstruction. Community composition varied strongly across habitats and associated environmental gradients. Species showed little overlap in their realized niche, suggesting resource partitioning, and a strong influence of environmental filtering driving community composition. Furthermore, phylogenetic clustering was observed in the most nitrogen-poor samples, supporting phylogenetic inheritance of adaptations in the group of N. guttata. This study showed that the studied free-living unicellular eukaryotes follow to community assembly rules similar to those known to determine plant and animal communities; the same may be true for much of the huge functional and taxonomic diversity of protists.
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Ecossistema , Sphagnopsida , Animais , Ecologia , Filogenia , PlantasRESUMO
Ecosystems are increasingly prone to climate extremes, such as drought, with long-lasting effects on both plant and soil communities and, subsequently, on carbon (C) cycling. However, recent studies underlined the strong variability in ecosystem's response to droughts, raising the issue of nonlinear responses in plant and soil communities. The conundrum is what causes ecosystems to shift in response to drought. Here, we investigated the response of plant and soil fungi to drought of different intensities using a water table gradient in peatlands-a major C sink ecosystem. Using moving window structural equation models, we show that substantial changes in ecosystem respiration, plant and soil fungal communities occurred when the water level fell below a tipping point of -24 cm. As a corollary, ecosystem respiration was the greatest when graminoids and saprotrophic fungi became prevalent as a response to the extreme drought. Graminoids indirectly influenced fungal functional composition and soil enzyme activities through their direct effect on dissolved organic matter quality, while saprotrophic fungi directly influenced soil enzyme activities. In turn, increasing enzyme activities promoted ecosystem respiration. We show that functional transitions in ecosystem respiration critically depend on the degree of response of graminoids and saprotrophic fungi to drought. Our results represent a major advance in understanding the nonlinear nature of ecosystem properties to drought and pave the way towards a truly mechanistic understanding of the effects of drought on ecosystem processes.
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Mudança Climática , Secas , Fungos/fisiologia , Plantas/microbiologia , Áreas Alagadas , Água Subterrânea , Consumo de Oxigênio , Microbiologia do Solo , Simbiose , Água/análiseRESUMO
Since the first environmental DNA surveys, entire groups of sequences called "environmental clades" did not have any cultured representative. LKM74 is an amoebozoan clade affiliated to Dermamoebidae, whose presence is pervasively reported in soil and freshwater. We obtained an isolate from soil that we assigned to LKM74 by molecular phylogeny, close related to freshwater clones. We described Mycamoeba gemmipara based on observations made with light- and transmission electron microscopy. It is an extremely small amoeba with typical lingulate shape. Unlike other Dermamoebidae, it lacked ornamentation on its cell membrane, and condensed chromatin formed characteristic patterns in the nucleus. M. gemmipara displayed a unique life cycle: trophozoites formed walled coccoid stages which grew through successive buddings and developed into branched structures holding cysts. These structures, measuring hundreds of micrometres, are built as the exclusive product of osmotrophic feeding. To demonstrate that M. gemmipara is a genuine soil inhabitant, we screened its presence in an environmental soil DNA diversity survey performed on an experimental setup where pig cadavers were left to decompose in soils to follow changes in eukaryotic communities. Mycamoeba gemmipara was present in all samples, although related reads were uncommon underneath the cadaver.
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Amebozoários/classificação , Amebozoários/crescimento & desenvolvimento , Meio Ambiente , Estágios do Ciclo de Vida , Filogenia , Amoeba/classificação , Amoeba/citologia , Amebozoários/genética , Amebozoários/ultraestrutura , Animais , Biodiversidade , Cadáver , Membrana Celular , DNA de Protozoário/genética , Água Doce/parasitologia , Sequenciamento de Nucleotídeos em Larga Escala/métodos , Microscopia Eletrônica de Transmissão , Organelas/ultraestrutura , RNA Ribossômico 18S/genética , Solo/parasitologia , Suínos/parasitologia , Suíça , Trofozoítos/crescimento & desenvolvimentoRESUMO
Decomposing cadavers modify the soil environment, but the effect on soil organisms and especially on soil protists is still poorly documented. We conducted a 35-month experiment in a deciduous forest where soil samples were taken under pig cadavers, control plots and fake pigs (bags of similar volume as the pigs). We extracted total soil DNA, amplified the SSU ribosomal RNA (rRNA) gene V9 region and sequenced it by Illumina technology and analysed the data for euglyphid testate amoebae (Rhizaria: Euglyphida), a common group of protozoa known to respond to micro-environmental changes. We found 51 euglyphid operational taxonomic units (OTUs), 45 of which did not match any known sequence. Most OTUs decreased in abundance underneath cadavers between days 0 and 309, but some responded positively after a time lag. We sequenced the full-length SSU rRNA gene of two common OTUs that responded positively to cadavers; a phylogenetic analysis showed that they did not belong to any known euglyphid family. This study confirmed the existence of an unknown diversity of euglyphids and that they react to cadavers. Results suggest that metabarcoding of soil euglyphids could be used as a forensic tool to estimate the post-mortem interval (PMI) particularly for long-term (>2 months) PMI, for which no reliable tool exists.
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Cercozoários/genética , Florestas , Mudanças Depois da Morte , Solo/parasitologia , Animais , Cercozoários/classificação , Código de Barras de DNA Taxonômico , Sequenciamento de Nucleotídeos em Larga Escala , Modelos Animais , Filogenia , RNA Ribossômico , SuínosRESUMO
The authors wish to make the following corrections to this paper [...].
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Rising temperatures in the Arctic affect soil microorganisms, herbivores, and peatland vegetation, thus directly and indirectly influencing microbial CH4 production. It is not currently known how methanotrophs in Arctic peat respond to combined changes in temperature, CH4 concentration, and vegetation. We studied methanotroph responses to temperature and CH4 concentration in peat exposed to herbivory and protected by exclosures. The methanotroph activity was assessed by CH4 oxidation rate measurements using peat soil microcosms and a pure culture of Methylobacter tundripaludum SV96, qPCR, and sequencing of pmoA transcripts. Elevated CH4 concentrations led to higher CH4 oxidation rates both in grazed and exclosed peat soils, but the strongest response was observed in grazed peat soils. Furthermore, the relative transcriptional activities of different methanotroph community members were affected by the CH4 concentrations. While transcriptional responses to low CH4 concentrations were more prevalent in grazed peat soils, responses to high CH4 concentrations were more prevalent in exclosed peat soils. We observed no significant methanotroph responses to increasing temperatures. We conclude that methanotroph communities in these peat soils respond to changes in the CH4 concentration depending on their previous exposure to grazing. This "conditioning" influences which strains will thrive and, therefore, determines the function of the methanotroph community.
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Protists dominate eukaryotic diversity and play key functional roles in all ecosystems, particularly by catalyzing carbon and nutrient cycling. To date, however, a comparative analysis of their taxonomic and functional diversity that compares the major ecosystems on Earth (soil, freshwater and marine systems) is missing. Here, we present a comparison of protist diversity based on standardized high throughput 18S rRNA gene sequencing of soil, freshwater and marine environmental DNA. Soil and freshwater protist communities were more similar to each other than to marine protist communities, with virtually no overlap of Operational Taxonomic Units (OTUs) between terrestrial and marine habitats. Soil protists showed higher γ diversity than aquatic samples. Differences in taxonomic composition of the communities led to changes in a functional diversity among ecosystems, as expressed in relative abundance of consumers, phototrophs and parasites. Phototrophs (eukaryotic algae) dominated freshwater systems (49% of the sequences) and consumers soil and marine ecosystems (59% and 48%, respectively). The individual functional groups were composed of ecosystem- specific taxonomic groups. Parasites were equally common in all ecosystems, yet, terrestrial systems hosted more OTUs assigned to parasites of macro-organisms while aquatic systems contained mostly microbial parasitoids. Together, we show biogeographic patterns of protist diversity across major ecosystems on Earth, preparing the way for more focused studies that will help understanding the multiple roles of protists in the biosphere.
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Ecossistema , Solo , Biodiversidade , Eucariotos/genética , Água Doce , FilogeniaRESUMO
Methane oxidizing bacteria (methanotrophs) within the genus Methylobacter constitute the biological filter for methane (CH4) in many Arctic soils. Multiple Methylobacter strains have been identified in these environments but we seldom know the ecological significance of the different strains. High-Arctic peatlands in Svalbard are heavily influenced by herbivory, leading to reduced vascular plant and root biomass. Here, we have measured potential CH4 oxidation rates and identified the active methantrophs in grazed peat and peat protected from grazing by fencing (exclosures) for 18 years. Grazed peat sustained a higher water table, higher CH4 concentrations and lower oxygen (O2) concentrations than exclosed peat. Correspondingly, the highest CH4 oxidation potentials were closer to the O2 rich surface in the grazed than in the protected peat. A comparison of 16S rRNA genes showed that the majority of methanotrophs in both sites belong to the genus Methylobacter. Further analyses of pmoA transcripts revealed that several Methylobacter OTUs were active in the peat but that different OTUs dominated the grazed peat than the exclosed peat. We conclude that grazing influences soil conditions, the active CH4 filter and that different Methylobacter populations are responsible for CH4 oxidation depending on the environmental conditions.
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Microbiologia do Solo , Solo , Regiões Árticas , Herbivoria , Metano , Oxirredução , RNA Ribossômico 16S/genética , SvalbardRESUMO
Decomposing vertebrate cadavers release large, localized inputs of nutrients. These temporally limited resource patches affect nutrient cycling and soil organisms. The impact of decomposing cadavers on soil chemistry is relevant to soil biology, as a natural disturbance, and forensic science, to estimate the postmortem interval. However, cadaver impacts on soils are rarely studied, making it difficult to identify common patterns. We investigated the effects of decomposing pig cadavers (Sus scrofa domesticus) on soil chemistry (pH, ammonium, nitrate, nitrogen, phosphorous, potassium and carbon) over a one-year period in a spruce-dominant forest. Four treatments were applied, each with five replicates: two treatments including pig cadavers (placed on the ground and hung one metre above ground) and two controls (bare soil and bags filled with soil placed on the ground i.e. "fake pig" treatment). In the first two months (15-59 days after the start of the experiment), cadavers caused significant increases of ammonium, nitrogen, phosphorous and potassium (p<0.05) whereas nitrate significantly increased towards the end of the study (263-367 days; p<0.05). Soil pH increased significantly at first and then decreased significantly at the end of the experiment. After one year, some markers returned to basal levels (i.e. not significantly different from control plots), whereas others were still significantly different. Based on these response patterns and in comparison with previous studies, we define three categories of chemical markers that may have the potential to date the time since death: early peak markers (EPM), late peak markers (LPM) and late decrease markers (LDM). The marker categories will enhance our understanding of soil processes and can be highly useful when changes in soil chemistry are related to changes in the composition of soil organism communities. For actual casework further studies and more data are necessary to refine the marker categories along a more precise timeline and to develop a method that can be used in court.
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Mudanças Depois da Morte , Solo/química , Compostos de Amônio/análise , Animais , Biomarcadores/análise , Carbono/análise , Colorimetria , Concentração de Íons de Hidrogênio , Modelos Animais , Nitratos/análise , Nitrogênio/análise , Fósforo/análise , Potássio/análise , Análise Espectral , Suínos , Fatores de TempoRESUMO
Criminal investigations of suspected murder cases require estimating the post-mortem interval (PMI, or time after death) which is challenging for long PMIs. Here we present the case of human remains found in a Swiss forest. We have used a multidisciplinary approach involving the analysis of bones and soil samples collected beneath the remains of the head, upper and lower body and "control" samples taken a few meters away. We analysed soil chemical characteristics, mites and nematodes (by microscopy) and micro-eukaryotes (by Illumina high throughput sequencing). The PMI estimate on hair 14C-data via bomb peak radiocarbon dating gave a time range of 1 to 3 years before the discovery of the remains. Cluster analyses for soil chemical constituents, nematodes, mites and micro-eukaryotes revealed two clusters 1) head and upper body and 2) lower body and controls. From mite evidence, we conclude that the body was probably brought to the site after death. However, chemical analyses, nematode community analyses and the analyses of micro-eukaryotes indicate that decomposition took place at least partly on site. This study illustrates the usefulness of combining several lines of evidence for the study of homicide cases to better calibrate PMI inference tools.
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Osso e Ossos/química , Homicídio , Ácaros , Nematoides , Microbiologia do Solo , Solo/química , Adolescente , Adulto , Animais , Humanos , Mudanças Depois da Morte , Adulto JovemRESUMO
High animal and plant richness in tropical rainforest communities has long intrigued naturalists. It is unknown if similar hyperdiversity patterns are reflected at the microbial scale with unicellular eukaryotes (protists). Here we show, using environmental metabarcoding of soil samples and a phylogeny-aware cleaning step, that protist communities in Neotropical rainforests are hyperdiverse and dominated by the parasitic Apicomplexa, which infect arthropods and other animals. These host-specific parasites potentially contribute to the high animal diversity in the forests by reducing population growth in a density-dependent manner. By contrast, too few operational taxonomic units (OTUs) of Oomycota were found to broadly drive high tropical tree diversity in a host-specific manner under the Janzen-Connell model. Extremely high OTU diversity and high heterogeneity between samples within the same forests suggest that protists, not arthropods, are the most diverse eukaryotes in tropical rainforests. Our data show that protists play a large role in tropical terrestrial ecosystems long viewed as being dominated by macroorganisms.