Apusomonadida Aaron A. Heiss, Matthew W. Brown, and Alastair G. B. Simpson Contents Summary Classification ........................................................................... 2 Introduction ....................................................................................... 3 General Characteristics ........................................................................ 3 Occurrence .................................................................................... 8 Literature and History of Knowledge ......................................................... 8 Practical Importance .......................................................................... 9 Habitats and Ecology ............................................................................. 9 Characterization and Recognition ................................................................ 10 General Appearance ........................................................................... 10 Ultrastructure .................................................................................. 12 Life Cycle..................................................................................... 13 Systematics .................................................................................... 14 Maintenance and Cultivation ..................................................................... 14 Evolutionary History ............................................................................. 14 Internal Relationships ......................................................................... 14 Overall Phylogenetic Position ................................................................ 15 Implications for Eukaryote Evolution ........................................................ 16 Coda: Breviates and Ancyromonads ............................................................. 17 References ........................................................................................ 22 A.A. Heiss (*) Department of Invertebrate Zoology and RGGS, American Museum of Natural History, New York, NY, USA e-mail: [email protected] M.W. Brown (*) Department of Biological Sciences, Mississippi State University, Mississippi State, MS, USA e-mail: [email protected] A.G.B. Simpson (*) Department of Biology, Dalhousie University, Halifax, NS, Canada e-mail: [email protected] # Springer International Publishing Switzerland 2016 1 J.M. Archibald et al. (eds.), Handbook of the Protists, DOI 10.1007/978-3-319-32669-6_15-1 2 A.A. Heiss et al. Abstract Apusomonadida is a small group of free-living heterotrophic flagellates. Apusomonads are small (~5–20 μm long) gliding aerobes with two flagella. The dorsal cell membrane is underlain by a pellicle, which also supports a “skirt” of folded membrane that extends laterally/ventrally. The anterior flagellum is enclosed by a sleeve-like extension of the skirt system, forming a flexible proboscis. Apusomonas itself is a rounded cell with an anterior extension, the mastigophore, that contains the flagellar apparatus. All other apusomonads (usu- ally now assigned to the genera Amastigomonas, Chelonemonas, Manchomonas, Multimonas, Podomonas, and Thecamonas) are elongated and plastic and may form ventral pseudopodia. Apusomonas is a soil flagellate. Most other apusomonads that have been cultured to date are marine. Apusomonads are closely related to opisthokonts (e.g., animals and fungi), making them an impor- tant group for examining, for example, the origins of multicellularity. The genome of Thecamonas trahens encodes several proteins and pathways previ- ously considered specific to animals, including much of the integrin system, which functions in cell-cell communication and adhesion in metazoa. This chapter also briefly reviews breviates and ancyromonads, two groups of surface-associating flagellates that are (or may be) closely related to apusomonads and are of similar evolutionary significance. Breviates comprise three genera of small (~10–15 μm long) anaerobic cells that produce fine pseudopodia. Ancyromonads (synonym planomonads) comprise four genera of tiny (~5 μm long) flattened cells with an inflexible pellicle underlying most of the cell membrane and a battery of extrusomes in a lateral rostrum. Keywords Aerobe • Anaerobe • Ancyromonad • Apusomonad • Bacterivore • Breviate • Flagellate • Integrin • Opisthokonts • Protozoa • Thecamonas Summary Classification • Apusomonadida ••Apusomonadidae ••• Apusomonadinae (Apusomonas, Manchomonas) ••• Thecamonadinae (Thecamonas, Chelonemonas) ••• Amastigomonas (Amastigomonas) ••• Multimonas (Multimonas) ••• Podomonas (Podomonas) [Other Apusomonadida: “Thecamonas” oxoniensis] • Breviatea (Breviata, Subulatomonas, Pygsuia, Lenisia) • Ancyromonadida (= Planomonadida) •• Ancyromonadidae (Ancyromonas, Nutomonas) Apusomonadida 3 •• Planomonas (Planomonas) •• Fabomonas (Fabomonas) Introduction General Characteristics Apusomonadida is a group of small free-living heterotrophic flagellates that glide on surfaces. All known apusomonads have two flagella, with the anterior flagellum surrounded by a membranous “sleeve” that extends from the main cell body. The combined flagellum-sleeve apparatus forms a highly mobile proboscis, which is a primary characteristic of the group (Karpov and Myľnikov 1989). The posterior flagellum runs underneath the cell venter (ventral face), on the left side of the cell. Pseudopodia, which are used for feeding, are produced from the ventral region of the cell in some members of the group. The dorsal cell membrane is underlain by a pellicle, which continues into a ventrally projecting “skirt” on the sides of the cell, and which is continuous with the proboscis sleeve (Fig. 1). Apusomonads are currently divided into at least five main phylogenetic groups, based on molecular and morphological data of cultured strains (Cavalier-Smith and Chao 2010; Heiss et al. 2015): (i) Apusomonadinae, containing the genera Apusomonas and Manchomonas; (ii) the genus Podomonas; (iii) the genus Multimonas; (iv) Thecamonadinae, including the genus Chelonemonas and the majority of members of the genus Thecamonas; and (v) the single freshwater species “Thecamonas” oxoniensis (Figs. 1 and 2; Table 1). Another genus, Amastigomonas sensu stricto (see below), is of uncertain position relative to other apusomonads. The most distinctive genus is Apusomonas, which has an inflexible, rounded body and an extended “mastigophore” that contains both the proboscis and the flagellar apparatus (Karpov and Myľnikov 1989; Vickerman et al. 1974; Figs. 1a and 2d). The other genera contain more elongate, flexible cells, with the flagellar apparatus positioned within the anterior end of the main cell body. The morphological differences between them are often subtle, and until recently all apusomonads other than Apusomonas were assigned to the genus Amastigomonas (a practice continued by some authors: Karpov 2011;Myľnikov and Myľnikova 2012). Apusomonads have an important phylogenetic position within the eukaryote tree of life. They are amongst the closest relatives of Opisthokonta, the “supergroup” that includes both animals and fungi (Brown et al. 2013; Burki et al. 2016; Cavalier-Smith and Chao 1995;Cavalier-Smithetal.2014; Derelle and Lang 2012;Heetal.2014; Kim et al. 2006;Papsetal.2013; Torruella et al. 2012, 2015). This suggests that apusomonads are important for understanding the origins of multicellularity in animals and fungi. In particular, the genome of the apusomonad Thecamonas trahens encodes most components of the integrin machinery critical to cell adhesion in animals (Seb- é-Pedrós et al. 2010). Thecamonas also has a more complex flagellar apparatus cytoskeleton than that seen in opisthokonts, and this sheds light on the deep-level evolution of the cytoskeletal architecture in extant eukaryotes (Heiss et al. 2013b). 4 A.A. Heiss et al. abacroneme anterior flagellum sleeve acroneme tusk mastigophore anterior flagellum sleeve proboscis proboscis skirt posterior flagellum cell lateral body pseudopodium posterior flagellum acroneme trailing pseudopodium Fig. 1 Appearance by light microscopy of living apusomonads. (a) Apusomonas proboscidea; (b) Thecamonas trahens. Nuclei are light grey; mitochondria are dark grey. Scale bar in (b) = 2 μm for both drawings Occurrence The majority of known apusomonads are marine; however, Apusomonas occurs in soil and “Thecamonas” oxoniensis was isolated from the surface of a terres- trial plant, both being essentially freshwater organisms (Cavalier-Smith and Chao 2010). The original account of Amastigomonas (see below) was also of a freshwater organism (de Saedeleer 1931). Apusomonads are one of the most frequently encountered groups of heterotrophic flagellates in microscopy studies of marine sediments (Patterson and Lee 2000), though almost always low in cell number. Literature and History of Knowledge The scientific history of apusomonads extends back a century, although the group was united less than three decades ago. The first described apusomonad was originally called Rhynchomonas mutabilis (Griessmann 1913), although it was not recognized as an apusomonad until almost 80 years later (Larsen and Patterson 1990; Apusomonadida 5 Fig. 2 Light (a–d) and scanning electron (e–i) micrographs of apusomonads. Panels (a–d) are differential interference contrast images of living cells: (a) Thecamonas trahens without prominent pseudopodia but with visible “tusk” (T); (b) Thecamonas trahens with prominent trailing 6 A.A. Heiss et al. true Rhynchomonas organisms are kinetoplastids – see chapter “▶