Samuel S. Bowser

The New Higher Level Classification of Eukaryotes with Emphasis on the Taxonomy of Protists

Abstract. This revision of the classification of unicellular eukaryotes updates that of Levine et al. (1980) for the protozoa and expands it to include other protists. Whereas the previous revision was primarily to incorporate the results of ultrastructural studies, this revision incorporates results from both ultrastructural research since 1980 and molecular phylogenetic studies. We propose a scheme that is based on nameless ranked systematics. The vocabulary of the taxonomy is updated, particularly to clarify the naming of groups that have been repositioned. We recognize six clusters of eukaryotes that may represent the basic groupings similar to traditional “kingdoms.” The multicellular lineages emerged from within monophyletic protist lineages: animals and fungi from Opisthokonta, plants from Archaeplastida, and brown algae from Stramenopiles.

The revised classification of eukaryotes.

This revision of the classification of eukaryotes, which updates that of Adl et al. [J. Eukaryot. Microbiol. 52 (2005) 399], retains an emphasis on the protists and incorporates changes since 2005 that have resolved nodes and branches in phylogenetic trees. Whereas the previous revision was successful in re‐introducing name stability to the classification, this revision provides a classification for lineages that were then still unresolved. The supergroups have withstood phylogenetic hypothesis testing with some modifications, but despite some progress, problematic nodes at the base of the eukaryotic tree still remain to be statistically resolved. Looking forward, subsequent transformations to our understanding of the diversity of life will be from the discovery of novel lineages in previously under‐sampled areas and from environmental genomic information.

CBOL Protist Working Group: Barcoding Eukaryotic Richness beyond the Animal, Plant, and Fungal Kingdoms

A group of protist experts proposes a two-step DNA barcoding approach, comprising a universal eukaryotic pre-barcode followed by group-specific barcodes, to unveil the hidden biodiversity of microbial eukaryotes.

MORTALITY, PROTOPLASM DECAY RATE, AND RELIABILITY OF STAINING TECHNIQUES TO RECOGNIZE ‘LIVING’ FORAMINIFERA: A REVIEW

Non-vital staining, especially with rose Bengal, has been widely used in ecological studies to differentiate between the tests of dead (unstained) foraminifera from those presumed to be living at the time of collection (stained). Doubts have been expressed about staining methods because of the possibility that dead individuals may retain undecayed protoplasm for weeks or months after death; when stained, such individuals would be recorded as living. To assess the importance of such false positives, it is necessary to examine rates of mortality, and the modes of generation of empty tests, i.e., whether due to reproduction, growth stages (leaving empty tests during growth) or death. It can be argued that reproduction, ontogeny, and death through predation lead to tests devoid of protoplasm. Whereas reproduction may affect only a small proportion of the population of each species (due to high pre-reproductive mortality), predation in oxygenated environments may be responsible for the major part of that pre-reproductive mortality. In oxygenated environments, disease or adverse environmental conditions are most likely to lead to dead individuals having tests containing protoplasm. In dysaerobic/anoxic environments, predation by macrofauna may be excluded, so foraminifera die through other causes and thus more tests with dead protoplasm may be potentially available for staining. Therefore, for most other environments, the problem of staining dead individuals is almost certainly overstated. Furthermore, from comparative studies, it seems that the most commonly used technique (staining with rose Bengal) is as reliable as others. Now that new vital staining techniques, especially the use of fluorescent probes, are being introduced, it is timely for further objective comparative studies of all techniques to be made in order to evaluate data already gathered and to develop the best strategies for future ecological studies according to whether they are field-based or experimental.

The evolution of early Foraminifera

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.

Diversity, Nomenclature, and Taxonomy of Protists

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Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology

Abstract Our recent surveys of dysoxic and anoxic sites reveal that many of the common foraminiferal inhabitants sequester chloroplasts. Such species include: Nonionella stella , which dominates the laminated sediments of the silled Santa Barbara Basin and comprises up to 82% of the living assemblage when [O 2 ] is below 2 μM (∼0.04 ml/l); the closely related species Nonionellina labradorica , which occurs in oxygen-depleted, silled fjords of Sweden; Stainforthia fusiformis , which dominates dysoxic sediments of Norwegian fjords; and Bulimina elegantissima , which is abundant in a shallow-water oil seep site supporting the filamentous, sulfide-oxidizing bacteria Beggiatoa . The literature contains examples of at least eight Elphidium species and one species from each of three other foraminiferal genera (i.e., Haynesina , Nonion , Reophax ) that are known to sequester chloroplasts. These foraminifera are typically infaunal and/or may live under dysoxic conditions. Photosynthetic activity of the sequestered chloroplasts might provide oxygen to the host foraminifera, thereby enabling them to inhabit anoxic pore waters. However, given that most of the surveyed sites occur in the aphotic zone where light levels are too low to fuel photosynthesis, it is more likely that the host employs an as yet unidentified biochemical pathway associated with the sequestered chloroplasts. Additionally, these foraminifera have external test ornamentations that may facilitate separation of the chloroplasts from their algal prey. We discuss potential uses for these morphological features in interpreting the fossil record.

Benthic foraminiferal assemblages in Explorers Cove, Antarctica : A shallow-water site with deep-sea characteristics

Abstract During November and December 1993, we sampled foraminiferal populations living at a 25–28m deep site in Explorers Cove, McMurdo Sound, Antarctica, by means of an airlift suction apparatus and sediment coring. Mean standing stocks (stained specimens per 10cm2) were 8.55±2.60 (all specimens >1mm, 0–10cm layer), 62.1±27.5 (all specimens >500μm, 0–10cm layer), 483 (all specimens >63μm, 0–1cm layer) and 632 (all specimens >28μm, 0–1cm layer). The fauna comprises diverse taxa including both hard-shelled and soft-shelled forms. The coarser fractions (>1mm) are dominated by large agglutinated foraminifera, mainly “spheres” and domes (psammosphaerids, saccamminids, notodendrodiids), but also contain some large calcareous taxa (Cibicides, Pyrgo). The finer fractions (>500, >63, >28μm) yield numerous soft-bodied monothalamous foraminifera in addition to the more commonly studied calcareous and multilocular agglutinated forms. Many species adopt epifaunal or shallow infaunal (0–1cm layer) microhabitats but a few smaller ones are more deeply infaunal (>1cm). A variety of trophic strategies can be inferred from the limited available evidence. Some abundant large species (Crithionina spp., Gromia oviformis) may be shallow infaunal or epifaunal deposit feeders, but the most striking feature of the fauna is the conspicuous occurrence of large epifaunal species which appear to be suspension feeders (e.g. Astrammina, Astrorhiza, Notodendrodes, Cibicides). Some of these foraminifera can probably switch trophic mode, for example, from suspension feeding to osmotrophy in response to a fluctuating food supply. The Explorers Cove fauna includes a mix of wide-ranging and endemic species. The main features of the fauna are consistent with environmental similarities (uniformly low temperatures, physical tranquillity, episodic food inputs) between Explorers Cove and deeper water settings. In the Northern Hemisphaere, comparable faunas (i.e. those in which large agglutinated taxa are a conspicuous element) are found in deep sublittoral and fjordic areas (100–1000m), as well as at some bathyal and abyssal localities (down to several thousands of metres) which receive a substantial organic matter input from processes such as upwelling. Foraminifera probably play a major ecological role in these systems, particularly in trophic interactions and organic carbon cycling. Their success may depend on two main attributes. First, they possess extremely efficient food gathering organelles (reticulopodia) and second, they become quiescent when starved but can rapidly increase their metabolic rate when presented with food. Our SCUBA-accessible study site in Explorers Cove provides a unique opportunity to clarify the role that these important protists play in shallow Antarctic waters as well as in more remote deep-water environments.

Molecular data reveal high taxonomic diversity of allogromiid Foraminifera in Explorers Cove (McMurdo Sound, Antarctica)

Abstract Allogromiids are organic-walled or agglutinated, single-chambered Foraminifera, common in deep-sea and polar benthic communities. The simple forms and paucity of distinctive features make allogromiid identification difficult by traditional means. Molecular phylogenetic methods offer alternative tools for species identification and are used here to investigate allogromiid diversity. We obtained 135 partial small-subunit ribosomal DNA sequences of allogromiids collected in Explorers Cove, McMurdo Sound, Antarctica. In contrast to the 27 morphotypes identified, phylogenetic analysis revealed 49 molecular types (considered separate species) that differ by more than 5% of sequence divergence. The 49 genetic types form 28 molecular supra-groups that differ by more than 20% and probably represent distinct genera or families. Large genetic distances separating the molecular types indicate unexpectedly high taxonomic diversity. Comparison of our data with sequences of non-Antarctic allogromiids suggests that Explorers Cove species might be endemic and only distantly related to comparable northern hemisphere fauna.

PHYLOGENY OF ALLOGROMIID FORAMINIFERA INFERRED FROM SSU rRNA GENE SEQUENCES

Allogromiids are classically defined as a group of monothalamous, soft-walled foraminiferans. Recent morphological, cytological, and molecular studies, however, challenge this view, showing that the soft-walled allogromiids are closely related to naked athalamids and unilocular agglutinated foraminiferans. To establish the phylogenetic relationships among these three groups we obtained partial small-subunit ribosomal DNA sequences of 50 species and undetermined morphotypes, and compared them to other foraminiferal taxa. Phylogenetic analyses of our data show that allogromiids, athalamids and astrorhizids comprise an assemblage of 13 lineages branching together at the base of the foraminiferal tree. Among these lineages, two are represented by a single species and four comprise similar genera, while the remaining seven are heterogeneous groups composed of several species having different types of wall structure and different test morphologies. All lineages are relatively well supported, yet the relationships among them are not resolved. In view of our data, we propose to revise the definition of allogromiids to include all naked and testate unilocular granuloreticuloseans that diverged early in the evolution of Foraminifera.