Cercozoa is a diverse, increasingly well-characterized phylum of protists (Cavalier-Smith 1998) founded mainly on the basis of 18S rDNA phylogenies that revealed a phylogenetic relationship between a variety of gliding zooflagellates and filose amoebae and plasmodiophorid plant parasites (Cavalier-Smith 1996/7; Cavalier-Smith and Chao 1997). Its unity was later confirmed by actin trees (Keeling 2001), molecular synapomorphies (Archibald and Keeling 2004; Archibald et al. 2003; Bass et al. 2005; Cavalier-Smith 2002; Cavalier-Smith and Chao 2003), morphological synapomorphies (Cavalier-Smith et al. 2008, 2009), and combined 28S and 18S rDNA phylogenetic analyses (Moreira et al. 2007). Cercozoa probably diversified from an early phagotrophic, rhizopodial biflagellate (Cavalier-Smith 2003) to contain a vast array of phenotypes (Bass et al. 2009; Cavalier-Smith 1998), all but overwriting and obscuring ancestral morphological characters.
This diversity of cercozoan body forms includes filose testate amoebae (both scale-bearers like Euglypha and non-silicified ones like Pseudodifflugia), amoeboflagellate algae (e.g. Chlorarachnion), zooflagellates with pseudopodia and siliceous scales (e.g. Allas), diverse parasites (e.g. Ascetosporea, the syncytial Plasmodiophora, Pseudopirsonia), naked reticulose amoebae (e.g. Filoreta) testate reticulose amoebae (Gromia), colonial flagellate (e.g. some Spongomonas), plantonic swimming flagellates (e.g. Ebria), numerous small gliding flagellate (e.g. Sandona, Bodomorpha, Allapsa, Cavernomonas), helioflagellates (e.g. Aurigamonas), soft-bodied amoeboflagellates (e.g. Agitata, Cercomonas, Eocercomonas and Paracercomonas), and thecate or scaly amoeboflagellates that emit ventral pseudopods from a marked groove or cleft (e.g. Thaumatomonadida, 'Protaspis' (here renamed Protaspa), Ventrifissura), and even protists with axopodia (desmothoracids and phaeodarians). Recent studies show that many hitherto completely unknown organisms as well as those of previously uncertain affinity are actually Cercozoa (e.g. Bass et al. 2009; Burki et al. 2002; Chantangsi et al. 2008; Chantangsi and Hoppenrath and Leander 2006; Kuhn et al. 2000; Longet et al. 2004; Vickerman et al. 2005). Despite this great expansion of the group, phylum-specific environmental gene libraries reveal that many Cercozoa remain to be described (Bass and Cavalier-Smith 2004; Bass et al 2009; Howe et al. 2009).
Class Granofilosea Cavalier-Smith and Bass, 2009
Naked non-gliding biflagellate or non-flagellate heterotrophs with granular filopodia ancestrally stretched across substratrum.
Order Leucodictyida Cavalier-Smith, 1993
Family Massisteriidae Cavalier-Smith, 1993 (Genus Minimassisteria)
Infraphylum Monadofilosa Cavalier-Smith 1997 stat. n.
Ancestrally amoeboflagellates that glide on posterior flagellum only.
Class Metromonadea Cavalier-Smith, 2007
Here emended by adding Metopiida because metopiids resemble metromonads in two characters absent from sarcomonads with which they were formerly classified (and with which they do not group on trees): a dense extracellular surface coat and highly elongated extrusomes.
Revised diagnosis: Non-pseudopodial marine gliding biflagellate predators on the eukaryotes; non-thecate but with a dense single or double layered surface coat that may extend up flagella. Extrusomes highy elongated. (Genus Micrometopion)
Class Sarcomonadea Cavalier-Smith, 1993
Revised diagnosis: Gliding, ancestrally (and almost always) biflagellate gliding zooflagellates without theca, often amoeboid; extrusomes usually spherical or shortly ellipsoid. Bacterivores, except for Aurigamonas. Mainly inhabit freshwater and soil.
Order Cercomonadida Poche, 1913 emend. Grasse, 1952 and Karpov et al., 2006
Family Cercomonadidae Saville Kent, 1880 sensu Karpov et al., 2006 (Genus Paracercomonas)
Order Pansomonadida Vickerman, 2005
Family Agitatidae Cavalier-Smith and Bass, 2009 (in Bass et al. 2009) (Genus Agitata)
Order Glissomonadida Howe et al. 2009
Family Sandonidae Howe et al., 2009 (Genus Neoheteromita)
Class Thecofilosea Cavalier-Smith, 2003 em.
Revised diagnosis; Ancestrally with robust organic extracellular theca (unlike most other Cercozoa which are usually naked or with scales), ventral filose pseudopodia, and two flagella with divergent centrioles; ancestrally benthic flagellates gliding on posterior flagellum only, emitting filose pseudopodia from ventral groove, but some secondarily planktonic swimmers amongst which ebriids have lost pseudopodia; flagella secondarily lost in Rhizaspididae and the tectofilosid testate amoebae (i.e. Amphitremidae Poche, 1913; Pseudodifflugiidae De Saedeleer, 1934; Chlamydophryidae De Saedeleer, 1934; Psammonobiotidae Golemansky, 1974; Volutellidae Sudzuki, 1979), and restricted to zoospores in phaeodarians; theca with two perforations for flagella in the flagellates, one perforation for pseudopodia in the thecate and most testate amoebae, two opposite perforations for pseudopodia in Amphitremidae, and three perforations in phaeodaria (thus also called Tripylea Hertwig, 1879), which have surrounded it by a pseudopodial net containing a pigmented phaeodium, thus converting it into a 'central capsule' (not homologous with that of Polycystinea of phylum Radiozoa). Silica scales absent (unlike many Imbricatea), but hollow silica endoskeleton in all ebriids and most phaeodarians.
Comments; We hereby emend the class by including a new order of gliding zooflagellates, Ventricleftida, Botuliforma which has a robust theca like most Thecofilosea and ventral furrow (Chantangsi and Leander 2010) and its sister group Ebriida (where the 'theca' is only tenuous as in Cryothecomonas aestivalis and a groove is absent) (both having condensed interphase chromosomes like Protaspa), and also including Phaeodaria at subclass rank.
Phaeodaria Haeckel, 1879 stat.n. Cavalier-Smith
Diagnosis; With 'central capsule' (modified theca) perforated by large astrophylum and typically lateral parapylae; dark pigmented phaeodium in extracapsular protoplasmic region; usually with hollow silica endoskeleton. (Silicofilosea (Adl et al. 2005) was a pointless name change; and misleading as most Thecofilosea are non-silicified.)
Order Cryomonadida Cavalier-Smith, 1993 emended by adding Rhizaspididae because rDNA trees show Rhogostoma
within the cryomonad zooflagellates, so they evolved after the flagellate common ancestor of Ebriida and Cryomonadida by loss of flagella and are unrelated to Pseudodifflugia.
Family Rhizaspididae Skuja, 1948 orth. em. (redescribed paper) (Skuja mistakenly put Rhizaspis within euglenoids, even though euglenoids never have filopodia, and invariably have flagella, both unlike Rhizaspis, treating it nomenclaturally as a plant, and overlooked the much greater similarity to Rhogostoma noted here for the first time).
Revised diagnosis; Thecate amoebae with ventral cleft that emits filopodia, which anastomose as reticulopodia in one species; theca thin, flexible, laterally compressed, adherent throughout to cell surface, consisting of single smooth dense layer outside and scarcely thicker than the plasm membrane; thus with bilateral symmetry, unlike Chlamydophryidae De Saedeleer, 1934 and other Tectofilosida which are typically radially symmetric. Ventral cleft contrasts with the circular or oval ventral orifice of Tectofilosida. Type genus Rhizaspis Skuja, 1948; other genera Rhogostoma Belar, 1921; Capsellina Penard, 1909. Electron microscopy by Simtzis and Le Goff (1981); we accept their evidence that C. timida is a Rhogostoma and establish R. timida Cavalier-Smith comb. n. (Basionym Capsellina timida Brown, 1911)
Comments; De Saedeleer (1934) did not include any these in this Chlamydophryinae, placing Capsellina in Lobosa and ignoring Rhogostoma. Meisterfeld (2002) put Rhogostoma and Capsellina in Clamydophryidae, but ignored Rhizaspis, which prior to our present recognition of its close similarity to Rhogostoma, was placed with Protaspis (now Protaspa) in the invalid family Thaumatomastigaceae (Patterson and Zolffel 1991). Our trees show that Rhogostoma (and by implication Rhizaspis) is robustly related to Protaspa but than neither belongs in Thaumatomonadida, which is not even in the same class.
Family Protaspidae Cavalier-Smith, 1993
Constituent genera Protaspa Cavalier-Smith nom. n. (replacement name for Protaspis Skuja, 1939) and Cryothecomonas Thomsen, Buck, Bolt & Garrison, 1991. (Genus Protaspis)
Order Ventricleftida Cavalier-Smith (original paper)
Diagnosis; Strongly flattened oval zooflagellate with rigid theca without scales; two unequal flagella emerge subapically, often from apical notch, posterior flagellum used of gliding on surfaces; ventral cleft from which branched filose pseudopods emerge for feeding separate from and posterior to flagellar groove (unlike Thaumatomonadida and Auranticordis). Extrusomes. Contains Ventrifissura Chantangsi and Leander, 2010 and Verrucomonas, Chantangsi and Leander, 2010.
Comments; Our Bayesian tree shows these genera as a clade that is sister to all previously known Thecofilosea; on both Bayesian and ML trees neither branches within Tectofilosida as stated but not demonstrated by Chantangsi and Leander (2010). Therefore we do not accept their placement within Tectofilosida or suggested modification to its diagnosis. Nor are they sisters of Imbricatea and Glissomonadida respectively as in the undersampled tree that used too few nucleotides of Chantangsi and Leander (2010). Because trees conflict on their precise position it is premature to decide whether this order is ancestral to or sister of other thecofilosans. Nonetheless, this order is a morphologically defined monophyletic taxon and whether it is paraphyletic or holophyletic is immaterial to its taxonomic validity (see Cavalier-Smith (2010) for a refutation of the widespread but mistaken antipathy to paraphyletic taxa).
Etymology; venter L. belly; plus cleft E.; because of their ventral cleft.
Class Imbricatea Cavalier-Smith, 2003
Revised diagnosis; Cercozoa with often imbricate silica scales and their closest non-scaly relatives. Ancestral condition probably a gliding zooflagellate with two flagella with devergent centrioles, and relatively rigid pellicle (unlike most Sarcomonadea) that helped define a disinct ventral groove from which filose pseudopods extended, but without the dense extracellular theca of Thecofilosea or internal silica skeleton of ebriids and Phaeodaria. Flagellar transition region longer than in cercomonads and sainouroids; unlike them with dense distal plate but without the internal dense aggregates and elaborate extra structures opposite the thecal contact zone in cryomonads. Groove and flagella secondarily lost by euglyphids, centrioles multiplied and reoriented to make four posteriorly directed gliding flagella in Auranticordis, which also lost pseudopodia; centrioles independently made parallel in the thaumatomonads/spongomonad subclade.
Comments; Imbricatea, originally defined as comprising only Thaumatomonadida and Euglyphida, the two cercozoan orders with silica scales (Cavalier-Smith and Chao 2003), is hereby redefined phylogenetically to comprise the last common ancestor of these two groups plus all its multiform descendants. This revision of Imbricatea includes of the first time the non-scaly order Spongomonadida, a new non-scaly order Marimonadida (including the enigmatic amoeba Rhabdamoeba with a posteriorly biflagellate gliding phase (Rogerson et al. 1998), Auranticordis, and Pseudopirsonia) and two new genera (Peregrinia with a Nudifila without silica scales).
Order Spongomonadida Hibberd, 1983
Family Spongomonadidae Karpov, 1990 (Genus Spongomonas)
Order Thaumatomonadida Shirkina, 1987
Thaumatomonads are flagellates with a largely rigid surface covered by silica scales formed in vesicles attached to mitochondria, and which often emit ventral pseudopodia for feeding. We have discovered a novel largely non-flagellate freshwater amoeba that possesses two-tiered siliceous scales similar to but not identical with those of Gyromitus limax, a creeping pear-shaped cell with two anterior flagella arising from a small anterior depression and delicate pseudopodia arising from a posterior groove (Swale and Belcher 1975). When first isolated in Germany our new strain also showed two flagella in some cells but after months of culture these were no longer visible by light microscopy, though by whole mount electron microscopy we occasionally saw images suggestive of two short non-scale-bearing flagella. The largely amoeboid nature of our strain (now CCAP 1956/1), its usually different shape, and distinguishable scales make it a separate species from G. limax, but in the same genus given its homologous scale architecture. However, the scales of G. limax and our new species differ so substantially from those of the Gyromitus type species (G. disomatus) that we separate them both from Gyromitus as a new genus Peregrinia. Gyromitus 'disomatus' scales resemble an oval serviette ring: a laterally compressed, latticed hollow cylinder with strongly outrolled upper and lower rims and a sieve-like sheet across its lower surface (Nicholls 1979; Swale and Belcher 1974), markedly different from all other thaumatomonad scales. In contast, those of Peregrinia (= Gyromitus) limax comb. n. (Swale and Belcher 1975) and our new species Peregrinia clavideferens have two dissimilar upper and lower tiers connected by three vertical struts at each end, somewhat as in certain Thaumatomonas species. Peregrinia and Gyromitus differ in scale structure and in locomotion (being amoeboid creepers or planktonic swimmers respectively not flagellar gliders) from the core Thaumatomonadidae for which scale structures and sequences are now both known (i.e. Thaumatomonas, Allas, Thaumatomastix and Reckertia). We therefore establish a new family Peregriniidae to embrace Peregrinia and Gyromitus. Thaumatomonadidae are holophyletic on our trees and collectively sister to Peregrinia. This grouping of the new scaly amoeba Peregrinia as deep sister to Thaumatomonadidae shows that two-tier thaumatomonad scales are phylogenetically much more ancient than previously realised, going back in time close to when thaumatomonads separated from other imbricate lineages. Peregrinia and Reckertia sequences show that most of basal group T of Bass and Cavalier-Smith (2004) comprises deep branching thaumatomonads.
Family Peregriniidae Cavalier-Smith (original paper)
Diagnosis; Thaumatomonads with only oval two-tiered body scales and no flagellar scales; absence of spine scales and flagellar scales distinguishes them from Thaumatomastix; scales either symmetric ovals with heavily outturned upper and lower rims (Gyromitus) or asymmetric ovals with concave to flat lower surface and convex upper surface with rims more strongly laterally inrolled than at the ends (Peregrinia). In contrast to Thaumatomonas, flagellar pit apical not subapical and ventral, or cells so amoeboid as to lack defined shape; flagella not clearly differentiated into anterior and posterior; unlike Thaumatomonadidae no evidence for flagellar gliding; locomotion by swimming or slow amoeboid creeping.
Type genus; Peregrinia Cavalier-Smith gen. n.
Other genus; Gyromitus Skuja (1939).
Family Thaumatomonadidae Hollande, 1952
(The name Thaumatomastigaceae (Patterson and Zolffel 1991), is illegitimate under ICBN as as it lacked a Latin diagnosis and invalid under both ICBN and ICZN (which we apply to all Cercozoa) as it was a nomenclaturally superfluous synonym (equally invalid is Thaumatomastigidae: Vors 1992); Zhukov (1971) correctly attributed the family to Hollande but Ekebom et al. (1995/6) wrongly gave Patterson and Zolffel as authority (their use of Thaumatomonadidae was not incorrect, as Patterson et al. (2002)) wrongly thought).
Revised diagnosis; Biflagellate cells with ventral pseudopodia, long ventral posterior pointing flagellum used for gliding on surfaces (unlike Peregriniidae) and a much shorter anterior flagellum; siliceous scales formed in vesicles attached to mitochondria cover the rigid cell surface except for a ventral zone that emits pseudopodia for feeding; unlike Peregriniidae do not transform completely into an amoeba; all have oval or triangular two-tiered body scales, with an upper plate bearing species-specific perforations supported at the oval ends or triangle corners by discrete struts (unlike Gyromitus); upper plate lacks central cleft with inrolled sides (unlike Peregrinia); Thaumatomastix only additionally has long spine scales with near-circular or rounded triangular bases. Anterior flagellum naked (Thaumatomonas, Allas) or with small scales (Reckertia, Thaumatomastix).
Type genus: Thaumatomonas De Saedeleer, 1931
Other genera: Thaumatomastix, Allas, Reckertia, Hyaloselene
Order Marimonadida Cavalier-Smith & Bass, 2011 (original paper)
Diagnosis; Non-scaly and non-thecate marine zooflagellates. Biflagellate swimming cells (Pseudopirsonia: diatom parasites) or interstitial gliding zooflagellates with somewhat deformable, semi-rigid pellicle underlain by muciferous bodies and four posterior flagella associated with ventral cleft (Auranticordis), or amoeboflagellates with two gliding posterior flagella and a non-flagellate feeding stage with broad lobose fan like pseudopods (Rhabdamoeba). Differ from Euglyphida the absence of silica scales and presence of flagella, and from thaumatomonads (the only other gliding imbricates) by absence of scales. Includes Pseudopirsonia Kuhn et al., 2004; Auranticordis Chantangsi et al. 2008, and Rhabdamoeba Dunkerley, 1921.
Comments; The name Auranticordida (invalid as a taxon, being rankless and devoid of diagnosis) was used to label NC1 (i.e. Auranticordis, Pseudopirsonia and two environmental sequences) on a tree (Chantangsi et al. 2008), but none of these taxa was previously assigned to an order. Their distinctive characters and marked differences from Euglyphida, Thaumatomonadida, and Spongomonadida merit ordinal recognition irrespective of whether they are holophyletic sisters of euglyphids, or paraphyletic ancestors of euglyphids. Rhabdamoeba was omitted from Lee e al. (2002, pp 1302-1328). Incertae sedis within Imbricatea.
Etymology; mare L. sea, monas Gk. unit, because all known are marine zooflagellates.
Family Nudifilidae Cavalier-Smith (original paper)
Order Euglyphida Copeland, 1956, emend. Cavalier-Smith, 1997
Family Ovulinatidae Cavalier-Smith, 2011 (original paper)
Diagnosis; Filose amoebae with ovoid organic test, lacking scales or mineral particles, aperture round to oval; pseudopodia hyaline, sometimes branched, long, tapering to a point arising directly from aperture or from web of hyaline cytoplasm emergent from it. Differs from its sister family Paulinellidae by lackng silica scales or plastid-like enslaved cyanobacterium.
Comments; This new family is essential because our trees show that Ovulinata was previously wrongly classified in Pseudodifflugiidae (Thecofilosea) and must be transferred to Imbricatea and Euglyphida. It differs so radically from Paulinella that it cannot be included in the same family.
Type genus; Ovulinata Anderson, Rogerson & Hannah, 1997