The curse of taxonomic uncertainty in biogeographical studies of free-living terrestrial protists: a case study of testate amoebae from Amsterdam Island

Thierry Jean Heger, Edward Mitchell
2009
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Résumé

Aim A current debate in microbial biogeography contrasts two views concerning the distribution of free-living microorganisms. The first view assumes a ubiquitous distribution, while the second view assumes that at least some species have limited geographical distributions. We tested for limited geographical distributions by identifying testate amoebae morphospecies from an extremely remote oceanic island where the potential for endemism is high. Location Amsterdam Island, Indian Ocean. Methods Sixty moss and water samples collected from the top of the volcano to the lowland were investigated for their testate amoeba content. Due to taxonomical uncertainties among the Argynnia (Nebela) dentistoma species complex (including A. antarctica), we also performed light- and scanning electron microscopy investigations on the shell ultrastructure and biometric analysis on several specimens of this taxon. Results We identified a total of 43 testate amoeba taxa belonging to 15 genera. Only 4 testate amoeba taxa had previously been recorded on this island. Testate amoeba communities of Amsterdam Island are dominated by cosmopolitan ubiquitous euglyphid taxa such as Trinema lineare, Assulina muscorum and Corythion dubium. The length and width ranges for Argynnia dentistoma on Amsterdam Island overlap with other records of this species and of A. antarctica, suggesting that A. antarctica is not a distinct taxon. Main conclusions Although Amsterdam Island is among the most remote islands in the world, an extensive inventory of testate amoebae morphospecies provided no clear evidence for endemism. On the one hand, our detailed morphometic analysis of the Argynnia dentistoma complex revealed that A. antarctica, a morphospecies previously suggested to display endemism, cannot be confidently distinguished from the cosmopolitan morphospecies A. dentistoma. On the other hand, five morphotaxa could not be identified with certainty and might represent new species, potentially with limited distribution. These examples illustrate how taxonomical uncertainties undermine biogeographic studies of testate amoebae. In order to allow better interpretation of morphology-based testate amoeba distribution data, an assessment of genetic diversity among and within morphotaxa in relation to geographic distance for some common testate amoebae should be given high priority.

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Thierry Jean Heger, Edward Mitchell
2009
Article

Résumé

Official source

https://infoscience.epfl.ch/record/130120?ln=fr

À propos de ce résultat

Concepts associés (16)

Concepts associés

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Biogeography, Evolution and Diversity of Free-Living Protists

Thierry Jean Heger

Although widely recognized as essential actors of ecosystem processes and representing a significant part of the Earth's biodiversity, free-living protists are poorly known. Major questions concerning their diversity, ecology, and evolution remain completely unresolved, partly because our knowledge of their taxonomy, at each different levels, is still extremely limited. In this thesis, I used testate amoebae as model organisms to get insights into the diversity and biogeography of protists. Testate amoebae are a polyphyletic group of free-living protists that are characterized by a shell composed of proteinaceous, calcareous, or siliceous material. The shells are differentiated by their shapes and ultrastructures, allowing for the identification of morphospecies more easily than in the vast majority of other protists. However, the taxonomic validity of the characters used to define morphospecies and the true diversity of testate amoebae are largely unknown. We studied the taxonomy of cyphoderiid testate amoebae (Rhizaria: Euglyphida), by combining morphological and molecular genetic approaches (chapters 2 and 3). We used light- and scanning electron microscopy to analyze the shell ultrastructure and biometry of several Cyphoderia morphospecies and sequenced gene portions of the Cytochrome Oxidase Subunit 1 (COI) and nuclear small subunit rDNA (SSU). These analyses revealed that while several described species are morphologically distinct and well-supported by the genetic data, other species, such as Cyphoderia ampulla, represent a complex of cryptic or pseudo-cryptic species. The presence of cryptic or pseudo-cryptic Cyphoderia species illustrates the limits of a morphology-based approach for assessing protist diversity using only characters visible by light microscopy. DNA sequence analyses may allow for a better resolution for both species identification and diversity estimates, provided that appropriate genetic markers can be developed. Genetic marker development in protists is particularly challenging because their representation in the international genomic databases is still very limited. The SSU marker also allowed us to build an extensive phylogeny of eulgyhid testate amoebae. We then used this phylogeny as a framework to analyze macro-evolutionary processes in testate amoebae, in particular, how easily a species can cross an ecological barrier and colonize new habitats. The taxa included in our phylogeny occurred either in marine, marine supralittoral or freshwater habitats, and species of each habitat segregated into distinct sub-clades. This indicates that transitions between these environments occur only rarely in the course of evolution (chapter 4). A reliable taxonomy for microorganisms is not only an essential prerequisite for estimating species diversities, it would also be a key component to resolve the long-lasting debate of whether free-living microorganisms are strictly cosmopolitan, or whether at least some species have limited geographic distributions (chapter 1). We analyzed Arcellinida and Euglyphida testate amoeba communities from Amsterdam Island, one of the most remote islands in the world located in the Indian Ocean, to search for endemic species with limited geographic distributions (chapter 5). In macroorganisms, the degree of endemism is generally high in such remote islands. Our extensive inventory of testate amoeba morphospecies provided no clear evidence for endemism. However, given that the morphology-based species identification gives only a limited taxonomic resolution, we cannot exclude the presence of morphologically non-distinctive endemic species (cryptic species). Thus, such taxonomic uncertainties undermine biogeographical studies of testate amoebae and other protists. To circumvent taxonomical uncertainties in biogeographical studies, we analyzed the distribution of a morphologically highly distinctive testate amoeba, Nebela ansata (chapter 6). We report the presence of this species in Nova Scotia, Canada and at sites in New Jersey where it was initially described. An extensive literature survey further confirmed the absence of this species from both, the remaining North American continent as well as other continents. Together, these data provide an unusually convincing case of a free-living microorganism with a very limited distribution range along the temperate East American coast. Overall, my thesis illustrates how, in most cases, the current morphology-based species identification greatly underestimates testate amoeba diversity and calls for an improvement of the taxonomic resolution and reliability. The extension of the current taxonomy using molecular-genetic tools should greatly contribute to this task and also shed light on the debate on the distribution of protists and other microorganisms. Together, such studies will provide a first step towards a better understanding of the diversity and evolution of microorganisms and improve their utility as model organisms in both fundamental and applied questions.

EPFL2010

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Biogeography, Evolution and Diversity of Free-Living Protists

Thierry Jean Heger

EPFL2010