Kingdom PROTISTA Haeckel, 1886

Protist classification, following Adl et al. (2012).

© Copyright P.O'Donoghue, The University of Queensland

Figure reproduced from Adl et al. (2012). [reproduced with permission from Wiley: DOI: 10.1111/j.1550-7408.2012.00644.x]

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Introduction

The core of this section of the Australian Faunal Directory is the various catalogues of Protozoa generously supplied to Australian Biological Resources Study by Prof. Peter O'Donoghue of The University of Queensland. These include O'Donoghue (2010) Catalogue of free-living ciliates (Protozoa: Ciliophora) recorded from Australia; O'Donoghue (2010) Catalogue of testate amoebae (Protozoa) recorded from Australia; and O'Donoghue (2011) Catalogue of protozoan parasites recorded in Australia. Dr Brett and Mrs Moira Robinson contributed treatments of non-testate Amoebae.

PROTISTA
Taxonomic classification systems are intended to show phylogenetic relationships between life-forms, reflecting their evolution by descent. Many taxonomic characters have been used to show differences and similarities between organisms, moving from conventional phenotypic characters (such as morphology, biology, geography) to contemporary genotypic characters (DNA and protein characterisation). After several centuries of considered debate and informed revision, the taxonomic classification of organisms now generally adheres to a three-domain system; recognising the Archaebacteria, Eubacteria and Eukaryota as profoundly different organisms, nonetheless with common ancestry. Four kingdoms of Eukaryota (‘true-nucleated’ organisms) are generally recognised: the Protista, Fungi, Animalia and Plantae.

Unicellular eukaryotes
The kingdom Protista comprises unicellular eukaryotic organisms which exist as structurally and functionally independent individual cells (including those species which are gregarious or form colonies). None has adopted the multicellular somatic organisation characteristic of metazoan organisms. Instead, they have developed relatively complex subcellular features (membranes and organelles) that enable them to survive the rigours of their environments. The kingdom is not considered a natural assemblage of organisms but rather a classification of convenience, containing motile protozoal protists as well as non-motile algal and fungal protists. Early classification schemes recognised the higher taxon Protozoa (with a capital ‘P’), but this has recently been subsumed to the descriptor protozoa (with a small ‘p’) in deference to the recognition of Protista (or Protoctista) as a better collective supergroup. Protists exhibit enormous diversity in form and function, and it has been conservatively estimated that there are about 100,000 extant species. They are ubiquitous as free-living organisms in terrestrial and aquatic habitats and as symbionts (commensals, mutualists or parasites) of most animals and many plants. The diversity of protistan organisms is well appreciated both in terms of their structural heterogeneity, as well as their species richness and zoogeographic/biogeographic distribution.

Protista may be autotrophic (produce their own organic molecules), heterotrophic (derive organic molecules from external sources) or even mixotrophic (alternating between internal and external sources). Phototrophs (or photoautotrophs) synthesise their own organic molecules with energy derived from photosynthesis, while osmotrophs (or saprotrophs) take up dissolved nutrients across their cell membranes by passive and active transport or by pinocytosis. Phagotrophs (or holotrophs) ingest particulate material and use metabolic processes (catabolic decomposition and anabolic synthesis) to derive energy and organic molecules. They may be filter-feeders with simple-to-sophisticated oral structures to sweep food towards the mouth or they may be predatory (actively preying on other organisms) — being bactivorous (ingest bacteria), algivorous (ingest algae), herbivorous (ingest plant material), carnivorous (ingest other microscopic protists or zooplankton) or even histophagous (parasites invading and eating the tissues of larger organisms).

Microscopic cells
Most Protista are microscopic organisms — only a few grow to a size large enough to be visible to the naked eye. The unicellular Protista (and indeed all individual cells of metazoan organisms) are constrained to microscopic sizes because of the small distances over which macromolecules may diffuse (all parts of the cell must be accessible). The microscopic cell is therefore the basic unit of life.

All eukaryotic cells are chimeric; they contain genetic information from multiple ancestral lineages. Modern molecular genealogies have generated complex pictures of eukaryote genomes where ancient lateral gene transfers have tangled their evolutionary history. All eukaryotes have a true nucleus (= ‘eu-karyon’) whereby the genetic material is enclosed by a membrane — in contrast to archae- and eu-bacteria (formerly referred to collectively, but incorrectly, as ‘prokaryotes’) where the genetic material lies directly in the cytoplasm. The nuclear membrane of eukaryotic cells is confluent with other endomembrane systems, including endoplasmic reticulum (serving as a scaffold for ribosomes — the sites of protein synthesis) and dictyosomes (Golgi bodies where proteins are processed and packaged). Structural support is provided by cytoskeletal elements (microtubules and microfilaments) which are also involved in motility, by means of undulipodia (including flagella and cilia) or pseudopodia (involving temporary cellular extensions and cytoplasmic streaming), feeding (phagocytosis and pinocytosis) and nuclear division (nuclear spindle formation). Animals and plants divide by open mitosis (extranuclear spindle, with pole bodies) but most protists divide by closed mitosis (nuclear envelope does not breakdown, but contains internal spindles), with the exception of parabasalids and dinoflagellates (exhibit closed mitosis with external spindles). The serial endosymbiosis theory (SET) posits that eukaryotic cells serially acquired various endomembrane and organellar systems from endosymbiotic bacteria over long evolutionary history. Indeed, molecular biological studies have indicated that mitochondria may have originated from α-proteobacteria (similar to rickettsias) and chloroplasts from cyanobacteria. Not all extant protozoa possess the ‘full’ complement of eukaryotic organelles (some lack dictyosomes, some lack mitochondria, etc), thus their variable possession of such components makes them basal to eukaryote evolution, or intermediary between bacterial domains and eukaryotes (in some cases, making them the perfect missing links).

Classification schemes
The name ‘proto-zoa’ literally means ‘first animals’ and early classification systems grouped the protozoa with members of the animal kingdom due to their many similarities to eukaryotic metazoan cells. However, they were recognised as a discrete assemblage on the basis of their unicellularlity and were assigned to the taxon Protozoa which was considered basal to the Metazoa (they are invariably figured as the trunk of the animal tree of life — befitting their name as the ‘first animals’). Nonetheless, the members of the subkingdom Protozoa are quite disparate. Indeed, the taxon has never been considered a natural assemblage of organisms but rather one of convenience. Various classification schemes have been proposed for protozoan organisms. Since its inception in the 1880s, the Butschlian scheme recognising four major assemblages has dominated. Flagellates, amoebae, sporozoa and ciliates were characterised mainly on the basis of their unique morphological features.

• Sarcodina (amoebae) temporary extensions of the cell body or ‘false feet’
(with pseudopodia) (amoeboid movement with protoplasmic flow)
• Mastigophora (flagellates) elongate ‘whip-like’ extensions of the cell membrane
(with flagella*) (central axoneme of microtubules with 2 + 9 configuration)
• Infusoria (ciliates) small ‘hair-like’ extensions of the cell membrane
(with cilia*) (similar to flagella but with more complicated root system)
• Sporozoa (spore-formers) tiny undulatory ridges in cell membrane impart gliding motion
(mechanism unknown, may involve subpellicular microtubules)

[*The flagella and cilia of eukaryotes ‘undulate’ (dynein-walking along microtubules) rather than ‘rotate’ like the flagella of archae-/eu-bacterial organisms. Some authorities therefore reserve the term ‘flagellum’ for bacteria and recommend the term ‘cilium’ for eukaryotes, while others favour the collective term ‘undulipodia’ for eukaryotic flagella and cilia.]

Many attempts were made to reconcile the members of these basic but disparate groups into a small number of phyla formally recognised in a consensus classification system. A range of phenotypic characters were used to classify organisms: including morphological (cellular/subcellular, light/electron microscopic); behavioural (in vivo host specificity, life cycle, distribution, in vitro cultivation requirements); and biochemical (metabolic respiration/digestion, drug sensitivity/resistance, molecular structure/function) characteristics. Several decades ago, the Society of Protozoologists published a revised classification system (Levine et al. 1980) and an illustrated guide (Lee et al. 1985) to the protozoa; recognising eight main phyla, principally on the basis of morphology.

• Sarcomastigophora (flagellates and amoebae) most free-living, some symbiotic
• Labyrinthomorpha (cells glide on ectoplasmic network)parasitic on marine algae
• Ciliophora (ciliates, dikaryotic) most free-living, some symbiotic
• Apicomplexa (‘sporozoa’, apical complex present) parasitic in vertebrates/invertebrates
• Microspora (unicellular spores with polar tubes) parasitic in vertebrates/invertebrates
• Haplosporidia (spores without polar capsules) parasitic mainly in oysters
• Paramyxea (unique cells within cells configuration) parasitic mainly in oysters
• Myxozoa (multicellular spores with polar capsules) parasitic mainly in fish

Over the last two decades, classification schemes have adopted a broader perspective to encompass all unicellular protistan organisms, including traditional protozoal, algal and fungal groups as well as their intermediates. Ultrastructural studies identified many new assemblages with distinctive subcellular features (organelles, membranes and cytoskeletal elements), and contemporary molecular biological studies on gene and protein sequences are now facilitating comparative analyses and the construction of phylogenetic trees whose topologies better reflect evolutionary relationships. The Society of Protozoologists revised their guide to the protozoa (Lee et al. 2000) with the recognition of some 40 protistan phyla on the basis of genotypic and phenotypic characters. Lower taxonomic groupings (families, genera and species) are often well supported by comparative genotypic analyses, while their higher taxonomic affinities (orders, classes, phyla) are slowly being resolved amidst some controversy. The Society (now the International Society of Protistologists) recently published a revised classification of eukaryotes (Adl et al. 2012), which is outlined in the attachment, with emphasis given to ‘classical’ protozoan/protistan assemblages.

Key features

Archaeplastida (Plantae sensu lato) comprises plants and their relatives. Cells are often bikont (with two emergent flagella), have prominent cell walls and possess chloroplasts surrounded by two membranes. They are divided into:
• Rhodophyta (Rhodophyceae) marine red algae, including many seaweeds; and
• Chloroplastida (Viridiplantae) ‘green plants’ including green algae (aquatic) and embryophytes (land plants)

SAR (supergroup with name derived from acronym for constituent groups, namely Stramenopiles, Alveolata, Rhizaria)

• Stramenopiles (Heterokonta) comprises cells with heterokont (different shaped) flagella and possessing chloroplasts surrounded by four membranes. Most are algae (ranging from multicellular kelp to unicellular diatoms), oomycetes (water moulds) and some peculiar protists (opalines).
• Opalinids are multi-flagellated cells which appear opalescent under white light. They are endosymbiotes in anurans.

• Alveolata comprises cells with cortical alveoli, apparent as flattened vesicles supporting the cell membrane and typically forming a flexible pellicle. Constituent groups are diverse and include:
• Dinoflagellates with ‘mesokaryotic’ nuclei (lacking histones, nucleosomes and chromosomes remain condensed during interphase). Mostly free-living aquatic autotrophs (with chloroplasts), some parasitic heterotrophs of zooplankton, filamentous algae, crustaceans and fishes.
• Perkinsids are parasitic flagellates; some cause disease in wild and farmed molluscs.
• Ciliophorans swim by means of hair-like cilia but they are characterized more by the possession of two types of nuclei (vegetative macronuclei and reproductive micronuclei).
• Apicomplexans are obligate intracellular parasites with a distinctive apical complex of organelles to facilitate entry into host cells.

• Rhizaria are mostly amoebae with fine pseudopodia (simple, branching or anastomosing). Many produce shells or skeletons (contributing to the fossil record). There are two main groups:
• Cercozoa comprises amoebae and flagellates that feed by means of filose pseudopods. The euglyphids form shells of siliceous scales/plates and are commonly found in aquatic and terrestrial habitats. Several groups of parasites are also represented: notably ascetosporans found as histozoic or coelozoic parasites of aquatic invertebrates (including the haplosporidia which form unicellular spores containing several dense organelles (known as haplosporosomes) and the paramyxea which form unique spore-within-spore arrangements in oysters).
• Retaria contains the Foraminifera (‘forams’) and Radiolaria (Radiozoa). Most forams are aquatic and they form thin reticulopodial nets for catching food and usually have an external shell or test made of calcium carbonate or agglutinated sediment particles. Most Radiolaria are zooplanktonic and form radial axopodia and intricate mineral skeletons.

Excavata contains a variety of free-living and symbiotic unicellular eukaryotes, most having flagella and a conspicuous ventral feeding groove. There are three main groups:
• Heterolobosea (Percolozoa) are typically amoeboid but they can transform between amoeboid, flagellate and encysted stages (collectively referred to as amoebo-flagellates, schizopyrenids or vahlkampfids). Most are found as bactivores in soil, water or faeces. They were traditionally considered lobose amoebae, but do not form true lobopodia and advance by eruptive waves
• Metamonads are anaerobic amitochondriate flagellates found as symbiotes in many animals. They include the retortamonads, diplomonads, parabasalids and oxymonads. All have basal bodies in characteristic groups of four, often associated with the nucleus, forming a karyomastigont.
• Euglenozoans have flagella with unique ultrastructural characteristics. In addition to the normal supporting axoneme, they contain a paraxonemal rod with a tubular and/or latticed structure. There are two main subgroups: the euglenoids with two flagella in an apical pocket, and the kinetoplastids with prominent extranuclear DNA (kinetoplast) and many with a recurrent flagellum forming an undulating membrane.

Amorphea (Unikonta) are eukaryotic cells that, for the most part, have a single emergent flagellum, or are non-flagellated amoebae. The cells are ‘without form’, not having a fixed shape unless restricted by external layer (cell wall, lorica, test, extracellular matrix). There are two main groups: the Amoebozoa (many amoeboid protists) and the Opisthokonta (animals, fungi and related forms).
• Amoebozoa are amoeboid protozoa that move by cytoplasmic streaming forming finger-like lobopodia. They are common in terrestrial and aquatic habitats, and some occur as symbiotes in other organisms. There are two main subgroups:
• Conosea (Variosea) comprises the archamoebae (amitochondriate amoebae) and mycetozoans (slime moulds).
• Lobosea contains the Tubulinea (cylindrical cells moving with streaming granular cytoplasm in cylindrical pseudopodia) and Flabellinea (flattened cells moving with clear leading hyaloplasm and slender subpseudopodia).

• Opisthokonta is a broad group of eukaryotes, including both the animal and fungus kingdoms. In at least one stage of their life-cycle, they form cells that are propelled by a single posterior flagellum.
• Holomycota (Nucletmycea) comprises the fungi and their relatives. They have cell walls that contain chitin, unlike the cell walls of plants, some protists and bacteria. Microsporidian* parasites which form unicellular spores with eversible polar tubes are now considered to be fungi.
• Holozoa (Metazoa/Animalia) are multicellular eukaryotic organisms that are heterotrophic, motile, have cells that lack rigid walls, and produce embryos that pass through a blastula stage. The group includes myxozoan* parasites which form multicellular spores with extrudible polar capsules similar to elements in Cnidaria.

*These parasite assemblages (Microspora and Myxozoa) are traditionally covered in most protozoology texts and they have been retained in this protistan database for historical comparative purposes.

General References

Adl, S.M., Simpson, A.G.B., Lane, C.E., Lukes, J., Bass, D., Bowser, S.S., Brown, M.W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., Le Gall, L., Lynn, D.H., McManus, H., Mitchell, E.A.D., Mozley-Stanridge, S.E., Parfrey, L.W., Pawlowski, J., Rueckert, S., Shadwick, L., Schoch, C.L., Smirnov, A. & Spiegel, F.W. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59: 429-493

Lee, J.J., Leedale, G.F. & Bradbury, P. (eds) 2000. An Illustrated Guide to the Protozoa. Lawrence, Kansas : Society of Protozoologists, Allen Press Inc. Vol. I.

Lee, J.J., Leedale, G.F. & Bradbury, P. (eds) 2000. An Illustrated Guide to the Protozoa. Lawrence, Kansas : Society of Protozoologists, Allen Press Inc. Vol. II.

Lee J.J., Hutner S.H. & Bovee E.C. 1985. An Illustrated Guide to the Protozoa. Society of Protozoologists, Allen Press 629 pp.

Levine, N.D., Corliss, J.O., Cox, F.E.G., Deroux, G., Grain, J., Honigberg, B.M., Leedale, G.F., Loeblich, A.R.III, Lom J., Lynn, D., Merinfeld, E.G., Page, F.C., Poljansky, G., Sprague, V., Vavra, J. & Wallace, F.G. 1980. A newly revised classification of the protozoa. Journal of Protozoology 27: 37-58

History of changes