staff

Maria Holzmann

Associate scientist in Molecular Systematics & Environmental Genomics

  • T: +41 22 379 30 84
  • office 4061B (Sciences III)
  • Cytochrome c oxidase barcodes for aquatic oligochaete identification: development of a Swiss reference database. PeerJ 2017 ;5():e4122. 10.7717/peerj.4122. 4122. PMC5723135.

    abstract

    Aquatic oligochaetes represent valuable indicators of the quality of sediments of watercourses and lakes, but their difficult identification based on morphological criteria compromises their more common use for eco-diagnostic analyses. This issue could be overcome by using DNA barcodes for species identification. A 10% threshold of cytochrome c oxidase (COI) divergence was proposed for differentiating between oligochaete species based on molecular and morphological data. A Swiss database of COI sequences of aquatic oligochaetes was initiated in 2012. The aim of this study is to complement the Swiss oligochaete database of COI sequences and to confirm the relevance of this threshold for species delimitation.

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  • Assessing SSU rDNA Barcodes in Foraminifera: A Case Study using Bolivina quadrata. J. Eukaryot. Microbiol. 2017 Sep;():. 10.1111/jeu.12471.

    abstract

    The Small Subunit Ribosomal RNA gene (SSU rDNA) is a widely used tool to reconstruct phylogenetic relationships among foraminiferal species. Recently, the highly variable regions of this gene have been proposed as DNA barcodes to identify foraminiferal species. However, the resolution of these barcodes has not been well established, yet. In this study, we evaluate four SSU rDNA hypervariable regions (37/f, 41/f, 43/e, and 45/e) as DNA barcodes to distinguish among species of the genus Bolivina, with particular emphasis on Bolivina quadrata for which ten new sequences (KY468817-KY468826) were obtained during this study. Our analyses show that a single SSU rDNA hypervariable sequence is insufficient to resolve all Bolivina species and that some regions (37/f and 41/f) are more useful than others (43/e and 45/e) to distinguish among closely related species. In addition, polymorphism analyses reveal a high degree of variability. In the context of barcoding studies, these results emphasize the need to assess the range of intraspecific variability of DNA barcodes prior to their application to identify foraminiferal species in environmental samples; our results also highlight the possibility that a longer SSU rDNA region might be required to distinguish among species belonging to the same taxonomic group (i.e., genus). This article is protected by copyright. All rights reserved.

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  • Taxonomic revision of freshwater foraminifera with the description of two new agglutinated species and genera. Eur. J. Protistol. 2017 May;60():28-44. S0932-4739(17)30078-0. 10.1016/j.ejop.2017.05.006.

    abstract

    Most foraminifera inhabit marine habitats, but some species of monothalamids have been described from freshwater environments, mainly from Swiss water bodies over 100 years ago. Recent environmental DNA surveys revealed the presence of four major phylogenetic clades of freshwater foraminifera. However, until now only one of them (clade 2) has been associated to a morphologically described taxon-the family Reticulomyxidae. Here, we present morphological and molecular data for the genera representing the three remaining clades. We describe two new agglutinated freshwater genera from China and the Netherlands, Lacogromia and Limnogromia, which represent clades 3 and 4, respectively. We also report the first ribosomal DNA sequences of the genus Lieberkuehnia, which place this genus within clade 1. Our study provides the first morphotaxonomic documentation of molecular clades of freshwater foraminifera, showing that the environmental DNA sequences correspond to the agglutinated monothalamous species, morphologically similar to those described 100 years ago.

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  • Molecular Phylogeny and Ecology of Textularia agglutinans d'Orbigny from the Mediterranean Coast of Israel: A Case of a Successful New Incumbent. PLoS ONE 2015 ;10(11):e0142263. 10.1371/journal.pone.0142263. PONE-D-15-21505. PMC4634767.

    abstract

    Textularia agglutinans d'Orbigny is a non-symbiont bearing and comparatively large benthic foraminiferal species with a widespread distribution across all oceans. In recent years, its populations have considerably expanded along the Israeli Mediterranean coast of the eastern Levantine basin. Despite its exceptionally widespread occurrence, no molecular data have yet been obtained. This study provides the first ribosomal DNA sequences of T. agglutinans complemented with morphological and ecological characterization, which are based on material collected during environmental monitoring of the hard bottom habitats along the Israeli Mediterranean coast, and from the Gulf of Elat (northern Red Sea). Our phylogenetic analyses reveal that all specimens from both provinces belong to the same genetic population, regardless their morphological variability. These results indicate that modern population of T. agglutinans found on the Mediterranean coast of Israel is probably Lessepsian. Our study also reveals that T. agglutinans has an epiphytic life mode, which probably enabled its successful colonization of the hard bottom habitats, at the Mediterranean coast of Israel, which consist of a diverse community of macroalgae. Our study further indicates that the species does not tolerate high SST (> 35°C), which will probably prevent its future expansion in the easternmost Mediterranean in light of the expected rise in temperatures.

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  • MOLECULAR PHYLOGENY OF CARTERINA SPICULOTESTA AND RELATED SPECIES FROM NEW CALEDONIA The Journal of Foraminiferal Research 44 (4), 440-450; 10.2113/gsjfr.44.4.440

    abstract

    Carterina spiculotesta is a common tropical benthic foraminifer characterized by fusiform or rod-like calcareous spicules covering the surface of the test. Because of this peculiar wall feature, the genus Carterina was separated from other foraminifera and placed in its own suborder (Caterinina) or order (Carterinida). However, there is no agreement about the origin of Carterina spicules, which are considered either as being secreted by the foraminiferal cell or as agglutinated foreign particles; if the latter case, the genus was placed in the order Trochamminida. Here, we attempted to resolve this controversy by analysis of genetic data from various carterinids collected in New Caledonia. We obtained seven complete and 47 partial small subunit (SSU) rDNA sequences. Our results show that all specimens of spicule-bearing Carterina cluster together in a strongly supported clade. Sister to this clade are undetermined lineages of trochamminid morphospecies. Together with its sister groups, the Carterina clade forms an independent lineage at the base of Globothalamea within the paraphyletic radiation of textulariids and robertinids. Its exact phylogenetic position was difficult to establish because the used SSU rRNA genes lack resolution. As long as experimental data do not contradict the hypothesis of a secreted origin for Carterina spicules, we propose to retain the ordinal status of the Carterina clade, and consider it as one of the orders of the class Globothalamea. In view of our study, the diversity of this order may be much higher than traditionally accepted, including several genera and species, many of them new to science.

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  • A plea for DNA barcoding of foraminifera Marine Biodiversity 44 (2), 213-221; DOI: 10.2113/gsjfr.44.1.62

    abstract

    DNA barcoding is the molecular identification of species using short, standardized gene sequences. Numerous applications of DNA barcoding in taxonomy, ecology, bioconservation, and biosafety contributed to a spectacular development of this initiative administered by the Consortium for the Barcode of Life (CBOL). Reference databases that assign DNA barcodes to particular morphospecies have been developed for almost all groups of animals, plants, and fungi, as well as some groups of protists (i.e., diatoms, ciliates, amoebae). However, such a database does not exist for foraminifera, despite large numbers of DNA sequences being available. To fill this gap, we initiated the Foram Barcoding (FB) project, whose objective is to create a curated molecular database for modern foraminifera. Each species included in our database is represented by one or several specimens, from which DNA was extracted and sequenced. Species entries include photos of processed specimens, taxonomic references, and DNA barcode sequences. A fragment of the 18S rRNA gene, commonly used in foraminiferal molecular studies, was chosen as the DNA barcode. We believe that the FB project will help resolve at least some misidentification problems that plague foraminiferal taxonomy. We also foresee its further applications in such domains of foraminiferal research as diversity assessment, ecology, biogeography, and biomonitoring. However, we are aware that the impact of the FB database depends mainly on its completeness and accuracy, and thus we appeal to the community of foraminiferologists to support this project by providing material for genetic studies and by contributing their taxonomic expertise in species identification and documentation.

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  • Molecular evidence for Lessepsian invasion of soritids (larger symbiont bearing benthic foraminifera). PLoS ONE 2013 ;8(10):e77725. 10.1371/journal.pone.0077725. PONE-D-13-03809. PMC3812231.

    abstract

    The Mediterranean Sea is considered as one of the hotspots of marine bioinvasions, largely due to the influx of tropical species migrating through the Suez Canal, so-called Lessepsian migrants. Several cases of Lessepsian migration have been documented recently, however, little is known about the ecological characteristics of the migrating species and their aptitude to colonize the new areas. This study focused on Red Sea soritids, larger symbiont-bearing benthic foraminifera (LBF) that are indicative of tropical and subtropical environments and were recently found in the Israeli coast of the Eastern Mediterranean. We combined molecular phylogenetic analyses of soritids and their algal symbionts as well as network analysis of Sorites orbiculus Forskål to compare populations from the Gulf of Elat (northern Red Sea) and from a known hotspot in Shikmona (northern Israel) that consists of a single population of S. orbiculus. Our phylogenetic analyses show that all specimens found in Shikmona are genetically identical to a population of S. orbiculus living on a similar shallow water pebbles habitat in the Gulf of Elat. Our analyses also show that the symbionts found in Shikmona and Elat soritids belong to the Symbiodinium clade F5, which is common in the Red Sea and also present in the Indian Ocean and Caribbean Sea. Our study therefore provides the first genetic and ecological evidences that indicate that modern population of soritids found on the Mediterranean coast of Israel is probably Lessepsian, and is less likely the descendant of a native ancient Mediterranean species.

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  • The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013 Jan;41(Database issue):D597-604. gks1160. 10.1093/nar/gks1160. PMC3531120.

    abstract

    The interrogation of genetic markers in environmental meta-barcoding studies is currently seriously hindered by the lack of taxonomically curated reference data sets for the targeted genes. The Protist Ribosomal Reference database (PR(2), http://ssu-rrna.org/) provides a unique access to eukaryotic small sub-unit (SSU) ribosomal RNA and DNA sequences, with curated taxonomy. The database mainly consists of nuclear-encoded protistan sequences. However, metazoans, land plants, macrosporic fungi and eukaryotic organelles (mitochondrion, plastid and others) are also included because they are useful for the analysis of high-troughput sequencing data sets. Introns and putative chimeric sequences have been also carefully checked. Taxonomic assignation of sequences consists of eight unique taxonomic fields. In total, 136 866 sequences are nuclear encoded, 45 708 (36 501 mitochondrial and 9657 chloroplastic) are from organelles, the remaining being putative chimeric sequences. The website allows the users to download sequences from the entire and partial databases (including representative sequences after clustering at a given level of similarity). Different web tools also allow searches by sequence similarity. The presence of both rRNA and rDNA sequences, taking into account introns (crucial for eukaryotic sequences), a normalized eight terms ranked-taxonomy and updates of new GenBank releases were made possible by a long-term collaboration between experts in taxonomy and computer scientists.

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  • CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol. 2012 ;10(11):e1001419. 10.1371/journal.pbio.1001419. PBIOLOGY-D-12-01686. PMC3491025.

    abstract

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  • Arnoldiellina fluorescens gen. et sp. nov.--a new green autofluorescent foraminifer from the Gulf of Eilat (Israel). Eur. J. Protistol. 2013 May;49(2):210-6. S0932-4739(12)00061-2. 10.1016/j.ejop.2012.08.005.

    abstract

    A new monothalamous (single-chambered) soft-walled foraminiferal species, Arnoldiellina fluorescens gen. et sp. nov., was isolated from samples collected in the Gulf of Eilat, Israel. The species is characterized by a small elongate organic theca with a single aperture of allogromiids. It is characterized by the emission of green autofluorescence (GAF) that has so far not been reported from foraminifera. Phylogenetic analysis of a fragment of the 18S rDNA indicates that the species is related to a group of monothalamous foraminiferans classified as clade I. Although the morphology of the new species is very different compared to the other members of this clade, a specific helix in 18S rRNA secondary structure strongly supports this position.

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  • Small subunit ribosomal DNA suggests that the xenophyophorean Syringammina corbicula is a foraminiferan. J. Eukaryot. Microbiol. ;50(6):483-7.

    abstract

    Xenophyophorea are giant deep-sea rhizopodial protists of enigmatic origins. Although species were described as Foraminifera or sponges in the early literature, the xenophyophoreans are currently classified either as a class of Rhizopoda or an independent phylum. To establish the phylogenetic position of Xenophyophorea, we analysed the small subunit (SSU) rRNA gene sequence of Syringammina corbicula Richardson, a newly described xenophyophorean species from the Cape Verde Plateau. The SSUrDNA analyses showed that S. corbicula is closely related to Rhizammina algaeformis, a tubular deep-sea foraminiferan. Both species branch within a group of monothalamous (single-chambered) Foraminifera, which include also such agglutinated genera as Toxisarcon, Rhabdammina, and Saccammina, and the organic-walled genera Gloiogullmia and Cylindrogullmia. Our results are congruent with observations of similar cytoplasmic organisation in Rhizammina and Syringammina. Thus, the Xenophyophorea appear to be a highly specialised group of deep-sea Foraminifera.

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  • The evolution of early Foraminifera. Proc. Natl. Acad. Sci. U.S.A. 2003 Sep;100(20):11494-8. 10.1073/pnas.2035132100. 2035132100. PMC208786.

    abstract

    Fossil Foraminifera appear in the Early Cambrian, at about the same time as the first skeletonized metazoans. However, due to the inadequate preservation of early unilocular (single-chambered) foraminiferal tests and difficulties in their identification, the evolution of early foraminifers is poorly understood. By using molecular data from a wide range of extant naked and testate unilocular species, we demonstrate that a large radiation of nonfossilized unilocular Foraminifera preceded the diversification of multilocular lineages during the Carboniferous. Within this radiation, similar test morphologies and wall types developed several times independently. Our findings indicate that the early Foraminifera were an important component of Neoproterozoic protistan community, whose ecological complexity was probably much higher than has been generally accepted.

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  • Freshwater foraminiferans revealed by analysis of environmental DNA samples. J. Eukaryot. Microbiol. ;50(2):135-9.

    abstract

    Sediment-dwelling protists are among the most abundant meiobenthic organisms, ubiquitous in all types of aquatic ecosystems. Yet, because their isolation and identification are difficult, their diversity remains largely unknown. In the present work, we applied molecular methods to examine the diversity of freshwater Foraminifera, a group of granuloreticulosan protists largely neglected until now. By using specific PCR primers, we detected the presence of Foraminifera in all sediment samples examined. Phylogenetic analysis of amplified SSU rDNA sequences revealed two distinct groups of freshwater foraminiferans. All obtained sequences branched within monothalamous (single-chambered), marine Foraminifera, suggesting a repeated colonization of freshwater environments. The results of our study challenge the traditional view of Foraminifera as essentially marine organisms, and provide a conceptual framework for charting the molecular diversity of freshwater granuloreticulosan protists.

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