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Mycamoeba gemmipara nov. gen., nov. sp., the First Cultured Member of the Environmental Dermamoebidae Clade LKM74 and its Unusual Life Cycle

2016-8-20, Blandenier, Quentin, Seppey, Christophe, Singer, David, Vlimant, Michèle, Simon, Anaele, Duckert, Clément, Lara, Enrique

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. In order 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 in order to follow changes in eukaryotic communities. M. gemmipara was present in all samples, although related reads were uncommon underneath the cadaver.

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Eight species in the Nebela collaris complex: Nebela gimlii (Arcellinida,Hyalospheniidae), a new species described from a Swiss raised bog

, Singer, David, Kosakyan, Anush, Pillonel, Amandine, Mitchell, Edward, Lara, Enrique

We describe here a new species of sphagnicolous testate amoeba found abundantly in the forested part of the Le Cachot peatland (Jura Mountains, Neuchâtel, Switzerland) based on microscopical observations (LM, SEM). The new species, called Nebela gimlii was placed in a phylogenetic tree based on mitochondrial cytochrome oxidase sequences (COI), and branched robustly within the N. collaris complex next to the morphologically similar N. guttata and N. tincta. It is however genetically clearly distinct from these two species, and differs morphologically from them by its smaller size and stouter shape of the shell. This new species completes the phylogeny of the Nebela collaris species complex, with now eight species described, mostly from peatlands and acidic forest litter, and further demonstrates the existence of an unknown diversity within testate amoebae. Improving the taxonomy of testate amoebae in peatlands and clarifying the ecology of newly discovered species should make these organisms even more valuable as bioindicator and for palaeoecological reconstruction.

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Microbial eukaryote communities exhibit robust biogeographical patterns along a gradient of Patagonian and Antarctic lakes

, Schiaffino, M. Romina, Lara, Enrique, Fernández, Leonardo D, Balagué, Vanessa, Singer, David, Seppey, Christophe C. W, Massana, Ramon, Izaguirre, Irina

Microbial eukaryotes play important roles in aquatic ecosystem functioning. Unravelling their distribution patterns and biogeography provides important baseline information to infer the underlying mechanisms that regulate the biodiversity and complexity of ecosystems. We studied the distribution patterns and factors driving diversity gradients in microeukaryote communities (total, abundant, uncommon and rare community composition) along a latitudinal gradient of lakes distributed from Argentinean Patagonia to Maritime Antarctica using both denaturing gradient gel electrophoresis (DGGE) and high-throughput sequencing (Illumina HiSeq). DGGE and abundant Illumina operational taxonomic units (OTUs) showed both decreasing richness with latitude and significant differences between Patagonian and Antarctic lakes communities. In contrast, total richness did not change significantly across the latitudinal gradient, although evenness and diversity indices were significantly higher in Patagonian lakes. Beta-diversity was characterized by a high species turnover, influenced by both environmental and geographical descriptors, although this pattern faded in the rare community. Our results suggest the co-existence of a ‘core biosphere’ containing reduced number of abundant/dominant OTUs on which classical ecological rules apply, together with a much larger seedbank of rare OTUs driven by stochastic and reduced dispersal processes. These findings shed new light on the biogeographical patterns and forces structuring inland microeukaryote composition across broad spatial scales.

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Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

, Mahé, Frédéric, de Vargas, Colomban, Bass, David, Czech, Lucas, Stamatakis, Alexandros, Lara, Enrique, Singer, David, Mayor, Jordan, Bunge, John, Sernaker, Sarah, Siemensmeyer, Tobias, Trautmann, Isabelle, Romac, Sarah, Berney, Cédric, Kozlov, Alexey, Mitchell, Edward, Seppey, Christophe V. W, Egge, Elianne, Lentendu, Guillaume, Wirth, Rainer, Trueba, Gabriel, Dunthorn, Micah

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.

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Dispersal limitations and historical factors determine the biogeography of specialized terrestrial protists

, Singer, David, Mitchell, Edward, Payne, Richard J, Blandenier, Quentin, Duckert, Clément, Fernández, Leonardo D, Fournier, Bertrand, Hernández, Cristián E, Granath, Gustaf, Rydin, Håkan, Bragazza, Luca, Koronatova, Natalia G, Goia, Irina, Harris, Lorna I, Kajukało, Katarzyna, Kosakyan, Anush, Lamentowicz, Mariusz, Kosykh, Natalia P, Vellak, Kai, Lara, Enrique

Recent studies show that soil eukaryotic diversity is immense and dominated by micro‐organisms. However, it is unclear to what extent the processes that shape the distribution of diversity in plants and animals also apply to micro‐organisms. Major diversification events in multicellular organisms have often been attributed to long‐term climatic and geological processes, but the impact of such processes on protist diversity has received much less attention as their distribution has often been believed to be largely cosmopolitan. Here, we quantified phylogeographical patterns in Hyalosphenia papilio, a large testate amoeba restricted to Holarctic Sphagnum‐dominated peatlands, to test if the current distribution of its genetic diversity can be explained by historical factors or by the current distribution of suitable habitats. Phylogenetic diversity was higher in Western North America, corresponding to the inferred geographical origin of the H. papilio complex, and was lower in Eurasia despite extensive suitable habitats. These results suggest that patterns of phylogenetic diversity and distribution can be explained by the history of Holarctic Sphagnum peatland range expansions and contractions in response to Quaternary glaciations that promoted cladogenetic range evolution, rather than the contemporary distribution of suitable habitats. Species distributions were positively correlated with climatic niche breadth, suggesting that climatic tolerance is key to dispersal ability in H. papilio. This implies that, at least for large and specialized terrestrial micro‐organisms, propagule dispersal is slow enough that historical processes may contribute to their diversification and phylogeographical patterns and may partly explain their very high overall diversity.

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Mycamoeba gemmipara nov. gen., nov. sp., the First Cultured Member of the Environmental Dermamoebidae Clade LKM74 and its Unusual Life Cycle

, Blandenier, Quentin, Seppey, Christophe V. W, Singer, David, Vlimant, Michèle, Simon, Anaële, Duckert, Clément, Lara, Enrique

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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High-throughput sequencing of litter and moss eDNA reveals a positive correlation between the diversity of Apicomplexa and their invertebrate hosts across alpine habitats

, Singer, David, Duckert, Clément, Heděnec, Petr, Lara, Enrique, Hiltbrunner, Erika, Mitchell, Edward

A high diversity of Apicomplexa was recently found in tropical soils presumably reflecting the diversity of their invertebrate hosts, but such patterns have not been explored in colder regions. We analysed the diversity of Apicomplexa and their potential metazoan hosts in litter and mosses collected in 11 different alpine habitats using an eDNA metabarcoding approach. The abundance and diversity of Apicomplexa phylotypes and of their potential invertebrate hosts were positively correlated. This confirms that eDNA metabarcoding is a useful tool to explore the unknown biodiversity of free-living eukaryotes, as well as potential host-parasite interactions. Future studies should aim at describing this diversity using a combination of morphological and molecular approaches.

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En garde! Redefinition of Nebela militaris (Arcellinida, Hyalospheniidae) and erection of Alabasta gen. nov.

, Duckert, Clément, Blandenier, Quentin, Kupferschmid, Fanny A. L, Kosakyan, Anush, Mitchell, Edward, Lara, Enrique, Singer, David

Molecular data have considerably contributed to building the taxonomy of protists. Recently, the systematics of Hyalospheniidae (Amoebozoa; Tubulinea; Arcellinida) has been widely revised, with implications extending to ecological, biogeographical and evolutionary investigations. Certain taxa, however, still have an uncertain phylogenetic position, including the common and conspicuous species Nebela militaris. A phylogenetic reconstruction of the Hyalospheniidae using partial sequences of the mitochondrial Cytochrome Oxidase Subunit 1 (COI) gene shows that N. militaris does not belong to genus Nebela, but should be placed in its own genus. The morphological singularities (strongly curved pseudostome and a marked notch in lateral view) and phylogenetic placement of our isolates motivated the creation of a new genus: Alabasta gen. nov. Based on their morphology, we include in this genus Nebela kivuense and Nebela longicollis. We discuss the position of genus Alabasta within Hyalospheniidae, and the species that could integrate this new genus based on their morphological characteristics.

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Soil protistology rebooted: 30 fundamental questions to start with

, Geisen, Stefan, Mitchell, Edward, Wilkinson, David M, Adl, Sina, Bonkowski, Michael, Brown, Matthew W, Fiore-Donno, Anna Maria, Heger, Thierry, Jassey, Vincent E.J, Krashevska, Valentyna, Lahr, Daniel J.G, Marcisz, Katarzyna, Mulot, Matthieu, Payne, Richard, Singer, David, Anderson, Roger O, Charman, Dan J, Ekelund, Flemming, Griffiths, Bryan S, Rønn, Regin, Smirnov, Alexey, Bass, David, Belbahri, Lassaâd, Berney, Cédric, Blandenier, Quentin, Blandenier, Quentin, Chatzinotas, Antonis, Clarholm, Marianne, Dunthorn, Micah, Feest, Alan, Fernández, Leonardo D, Foissner, Wilhelm, Fournier, Bertrand, Gentekaki, Eleni, Hájek, Michal, Helder, Johannes, Jousset, Alexandre, Koller, Robert, Kumar, Santosh, La Terza, Antonietta, Lamentowicz, Mariusz, Mazei, Yuri, Santos, Susana S, Seppey, Christophe V.W, Spiegel, Frederick W, Walochnik, Julia, Winding, Anne, Lara, Enrique

Protists are the most diverse eukaryotes. These microbes are keystone organisms of soil ecosystems and regulate essential processes of soil fertility such as nutrient cycling and plant growth. Despite this, protists have received little scientific attention, especially compared to bacteria, fungi and nematodes in soil studies. Recent methodological advances, particularly in molecular biology techniques, have made the study of soil protists more accessible, and have created a resurgence of interest in soil protistology. This ongoing revolution now enables comprehensive investigations of the structure and functioning of soil protist communities, paving the way to a new era in soil biology. Instead of providing an exhaustive review, we provide a synthesis of research gaps that should be prioritized in future studies of soil protistology to guide this rapidly developing research area. Based on a synthesis of expert opinion we propose 30 key questions covering a broad range of topics including evolution, phylogenetics, functional ecology, macroecology, paleoecology, and methodologies. These questions highlight a diversity of topics that will establish soil protistology as a hub discipline connecting different fundamental and applied fields such as ecology, biogeography, evolution, plant-microbe interactions, agronomy, and conservation biology. We are convinced that soil protistology has the potential to be one of the most exciting frontiers in biology.