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Unitat de Botànica, Departament de Biologia Animal, de Biologia Vegetal i d’Ecologia, Facultat de Ciències, Universitat Autònoma de Barcelona, 08193-Bellaterra (Barcelona), España
Matías J. Cafaro 2
Departamento de Biología, Universidad de Puerto Rico, Mayagüez, Puerto Rico 00681-9012
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ABSTRACT |
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We report the inedited occurrence of zygospores in symbiotic Asellariales (Zygomycota) from Puerto Rico and Dominican Republic. Two new species of Asellaria are described, Asellaria dactylopus and A. jatibonicua, both found in the hindgut of terrestrial isopods. The presence of spherical zygospores in the latter species represents a novelty for the order. The related gut-fungi Harpellales were known to produce sexual spores, characteristically conical or biconical. Order Asellariales is emended to include the description of zygospores. An undetermined species of Orchesellaria also is reported from the Caribbean. Comments are provided for each of the species as well as drawings and photographs to illustrate each taxon.
Key words: Caribbean, Collembola, Isopoda, symbiosis, taxonomy, Zygomycota, zygospores
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INTRODUCTION |
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, Cafaro 2005, Lichtwardt et al 2001, Nardi et al 2006). Some of these endosymbionts share particular characteristics such as those included within the ecological group "trichomycetes", organisms with filamentous structures, branched or not, attached to the chitinous gut lining of their hosts by means of cellular structures or secreted holdfast material (Lichtwardt 1986). This group of obligate gut symbionts comprises members of the protistan group Mesomycetozoa (Amoebidiales and Eccrinales) and Zygomycotan fungi (Asellariales and Harpellales), so it is not a natural group but a cluster of organisms sharing the same ecology and convergent morphology (Benny and O’Donnell 2000, Cafaro 2005, White et al 2006). At present the systematic position of trichomycetes is getting reorganized after an exhaustive revision (Lutzoni et al 2004, White et al 2006, Hibbett et al 2007).
All Asellariales have filamentous, branched thalli and reproduce asexually by arthrospore-like cells that disarticulate from their corresponding thallus (Lichtwardt and Manier 1978). The known species of this order inhabit the digestive tract of terrestrial, aquatic and marine isopods as well as springtails (Lichtwardt and Manier 1978, Lichtwardt et al 2001) and represent the most understudied group of gut fungi. Asellariales currently include three genera: Asellaria Poisson (1932), with nine species (including those reported here); Orchesellaria Manier ex Manier & Lichtw. (Manier and Lichtwardt 1969) with four described species; and Baltomyces Cafaro (1999), a monotypic genus. The later is placed provisionally within Asellariales because, according to some particular features, it might deserve a different classification (Cafaro 1999). The relationship that Asellariales establish with their hosts is not well understood because none of the known species have been cultured successfully, preventing the performance of physiological or ecological studies ex-situ. The relationship putatively is considered commensalistic (Lichtwardt 1986), according to the external absence of symptoms or differences between infected and noninfected hosts, whereas studies are needed to resolve this question.
The study of arthropod-gut symbionts in the Caribbean islands started with the record of an Eccrinales (Passalomyces compressus) from Grenada and Dominica (Lesser Antilles) found in the digestive tract of a Passalidae beetle (Thaxter 1920). A more recent article on trichomycetes (sensu lato) from Puerto Rico includes the report of four species of Harpellales, one marine Asellariales (Asellaria ligiae), two Eccrinales and two Amoebidiales, most of them cosmopolitan or neotropical widespread species (White et al 2000). We include here information concerning Asellariales from Puerto Rico and the Dominican Republic. Arthropod gut symbionts (trichomycetes), including Asellariales, previously were unknown for the Dominican Republic.
We also report the occurrence of zygospores in Asellariales when the only trichomycetes with documented sexual spores—zygospores—were before present the Harpellales (Lichtwardt et al 2001). The implication of this finding will be commented in the discussion because it might provide useful information for the classification of the Asellariales, for which no molecular data is available. We emend the diagnosis of order Asellariales to accommodate the description of zygospores in this taxon.
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MATERIALS AND METHODS |
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TAXONOMY |
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(=Asellariales Manier 1950, nom. inval.) emend Valle & Cafaro. Thalli branched and septate, attached to the hindgut cuticle of Isopoda or Collembola hosts by variously shaped holdfast cells, which is the distinguishing feature of genera and species within the order. Asexual reproduction by means of arthrospores, which disarticulate from the thallus. Terminal or intercalary spherical chlamydospores can be formed in some species as resistance asexual structures. Sexual reproduction involves the formation of spherical thick-walled zygospores, which arise after the formation of conjugation tubes.
New species –
Asellaria dactylopus L.G. Valle & Cafaro, sp. nov. FIGS. 1–7
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Thallus small, robust, 260–420 µm long, with main axis pinnately branched. Basal cell (C1) 23–37 x 12–20 µm, broadly obpyriform to broadly ellipsoid, with a slightly thick wall, with lobulate projections at the proximal end, covered by a skirt of hyaline holdfast material; various branches arising from the lower part of the basal cell; a single cell (C2) arising directly above the upper septum of the basal cell, obpyriform, typically smaller, giving rise to 2–4 verticillate branches that disarticulate into arthrospores. Arthrospores not regularly cylindrical but typically wider at the distal end, 12–20 µm long x 7–9.5 µm diam. Zygospores unknown. On the hindgut lining of isopods (Isopoda, Oniscidae).
Etymology.. Greek: dactyl- = finger, -pus = footed, referring to the lobulated basal cell.
Specimens examined.. PUERTO RICO. MAYAGÜEZ: University of Puerto Rico (RUM), prepared from Venezillo sp. (Armadilliidae), microscope slides PR-8-L15, 24-X-2006; PR-11-L1–L14, (HOLOTYPE: FH. PR-11-L2), 30-X-2006. Parque de los Próceres, prepared from Venezillo sp., microscope slides PR-24-L3, 29-XII-2006. DOMINICAN REPUBLIC. SANTO DOMINGO: Plaza de la Cultura, under vegetation debris and humic soil, prepared from Venezillo sp., microscope slides DR-8-L1–L3, 01-XII-2006.
Commentary..
This new species of Asellaria is easily separated from previously known species in the genus by the shape of the thallus (FIGS. 1
, 2, 5–7), characterized by short obovoid cells that disarticulate into arthrospores (FIG. 2, arrowheads), and especially by the basal cell, with digitated projections that contribute anchoring the thallus along with secreted holdfast material (FIGS. 1–4). The structure of the thallus and branching pattern is remarkably constant among individuals and localities. The small host (1.5–2.5 mm) might be responsible for the compressed structure of the fungus, which is actually the smaller known member within Asellaria, being comparable to the size of Orchesellaria species, which inhabit the tract of springtails (Collembola). The presence of thick-walled cells in the thallus (especially C1 and occasionally C2) (FIG. 5) is not known among other species of Asellariales but might have a biological significance because these likely have a major resistance to adverse conditions such as desiccation. Almost certainly the whole thallus becomes fragmented into detachable arthrospores, and at some point C1 might acquire the role of a diaspore (within extruded molt) and their thick-walls might provide them with a better defense to survive in the external environment until consumed.
Venezillo isopods were distributed in communities of numerous individuals in the interstice of humic soil but not where dense vegetation covered the surface, preferring uncompacted soils. Not all the explored communities presented infection, but the percentage of infestation within a population was relatively high (70–75%).
Asellaria jatibonicua L.G. Valle & Cafaro, sp. nov. FIGS. 8–24
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Thallus 600–1000 x 11–15 µm, with main axis longer than lateral ramifications. Verticillate branches usually 2–4, arising from each of the axial cells next to the upper septum, those growing from the lower region being longer (FIGS. 8–10); mature specimens sometimes showing profuse verticillate branching up to fourth order. Basal cell elongate-fusiform, 70–120(–140) x 14–20 µm, tapering to a small bulbous or campanulate proximal end, secreting sticky material accommodating to the substrate (FIGS. 9–11), with 1–6 pairs of ramifications, 8–12.5 µm diam, arising pinnately from the basal cell (FIG. 11). Arthrospores 15–34 x 6.5–11 µm, the terminal ones longer, rounded at the apex, the intercalary ones shorter, truncate at both ends, disarticulating first from distal branches, although even the cells from the main axis finally may become disarticulated. Zygospores spherical, 14–16 µm diam, with prominently thick walls, slightly ellipsoid in young phases, arising not directly from conjugation tubes (FIGS. 22–23) but on contiguous cells, always next to a septum (FIGS. 16–17, 19–21). On the hindgut lining of Littorophiloscia culebrae (Moore 1901) (FIG. 15) (Isopoda, Oniscidae, Philosciidae).
Etymology.. Local, referring to the Jatibonicu, a tribe of pre-Colombian Taíno people in Puerto Rico.
Specimens examined.. PUERTO RICO. CABO ROJO: Estancias de Miramar, in humic soil between rocks, prepared from Littorophiloscia culebrae (Philosciidae), microscope slides PR-2-L1–L7, PR-2-L-9, 12-X-2006. JAYUYA: state forest of Toro Negro, prepared from L. culebrae collected in humic soil, microscope slides PR-6-L1–L3, 14-X-2006. MAYAGÜEZ: University of Puerto Rico (RUM), prepared from L. culebrae, microscope slides PR-8-L2–L14 (PR-8-L10: Zygospores), PR-8-L16–7, 22-X-2006; PR-12-L1, 30-X-2006; PR-14-L1–L3 (zygospores), 02-IX-2006; PR-17-L1–L3, 15-IX-2006; PR-26-L1–L3 (HOLOTYPE: FH. PR-26-L3), prepared from L. culebrae collected in slopes and terrain with vegetation and humic soil, 02-XII-2006; Parque de los Próceres, PR-24-L1–L2, prepared from L. culebrae collected in garden terrain, 29-XII-2006.
Commentary..
This species closely resembles to Asellaria armadillidii Tuzet & Manier ex Manier (1968), which was described from different French species of the terrestrial isopod Armadillidium (Armadilliidae); the infestation was extended in lab conditions within diverse species of isopods of the Porcellionidae family (Tuzet and Manier 1953). The specimens we collected in Puerto Rico were found in the last portion of the hindgut lining of Littorophiloscia culebrae (Philoscidae) hosts. The same host was collected and dissected in Dominican Republic, but the fungi inquilines were absent. Morphologically, A. jatibonicua can be recognized by the basal cell (FIGS. 9–11), which is usually simple, fusiform-cylindrical, and slightly variable at the proximal end where it usually attenuates to a rounded end with secreted sticking holdfast material (FIGS. 9–10, 24). The proximal end occasionally does not attenuate but widens, as the external cell wall seems to expand into holdfast material, while the main inner membrane and cell content maintain the attenuated shape of most basal cells (FIG. 11). The holdfast of A. armadillidii can be identified by the projections it presents in the proximal end (Tuzet and Manier 1953). Also A. jatibonicua presents longer arthrospores (FIG. 18) than those reported for A. armadillidii (Tuzet and Manier 1953, Lichtwardt et al 2001). The ramification pattern in A. jatibonicua can be profuse in mature specimens, showing regions with a peculiar verticillate pattern (FIGS. 13–14, arrowheads), which often is not a true verticile but close unidirectional pinnate branches with the appearance of a verticile. When branches are fragmented into arthrospores and detached a footstep-like slit is observed in the supporting hypha, and when most of the branches have disarticulated, the step-like appearance is very characteristic (FIG. 13).
Undetermined species:. Orchesellaria sp. Specimens were found in the hindgut of Podurae Collembolans from a small pond organically polluted in Dominican Republic (DR-32-L1–L2, next to Sabana de la Mar, Hato Mayor, N19°02.273' W69°23.279', 08-XII-2006). Infection ratio was low among the springtail population, and few thalli were observed in each gut of the only two infested collembolans. Most of collembolans had already molted apparently, and the only specimens with fungal symbionts were those conserving the old chitinous skeleton on, just before loosing it. In the nearly-to-molt hindgut, branched thalli with few arthrospores (ca. 15'17.5 x 3.5 µm) were observed; even the basal cell was not clearly distinguishable and was not possible for the scant material to identify the species of Orchesellaria. We want to report the presence of this genus of Asellariales within Hispaniola because is it represents the first notice of Orchesellaria for the Caribbean islands.
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DISCUSSION |
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, Valle 2006), while thallial and sporic features may complement the information for classification. The peculiar digitate holdfast of A. dactylopus is unique among Asellariales, as well as the regular disposition of the thallial clavated cells. This species is probably widespread in Hispaniola and Puerto Rico, where the minute host was abundant, although not always easy to notice. The presence of this new species in other Caribbean islands, as well as in in Venezuela and Central America should be pursued in future surveys because resulting data might be of great interest for biogeographic analysis. The host, an unidentified species of Venezillo, is widely distributed in lowland areas of Puerto Rico and Dominican Republic. This genus has a circumtropical distribution, 20 species within Venezillo currently are known from the West Indies ( Jass and Klausmeier 2006). The second species, Asellaria jatibonicua, closely related to A. armadillidii, can be recognized also by its holdfast cell, usually campanulate, with a thick hyaline cell wall extending in the proximal region. Few specimens showed a basal cell not characteristically campanulate but with a cylindrical basal cell. The species was found associated with the Philoscidae isopod Littorophiloscia culebrae, which has been reported from diverse localities in Central and South America, as well as in other circumtropical areas around the globe (Schmalfuss 2003).
Production of zygospores.— –
Within the Asellariales sexual spores were unknown previously, although scalariform conjugations between different thalli of Asellaria ligiae from Hawaiian freshwater Ligia isopods were observed (Lichtwardt 1973). Indicia of sexuality from other described species of Asellaria have been observed by RW Lichtwardt (pers com) and MM White (pers comm), but the authors did not have enough information to describe the presence of sexual processes in those occasions. Spherical chlamydospores were reported by Lichtwardt and Moss (1984) on thalli of Orchesellaria pelta and O. mauguioi, a genus of Asellariales typically found in Collembolan hosts (Lichtwardt and Moss 1984). These chlamydospores closely resemble the zygospores we report here for Asellaria, thus we first identified the thick-walled, rounded structures as resistant spores until the observation of conjugations that denoted possible genetic interchange between conjugating thalli. In the case of Orchesellaria chlamydospores, thallial cells transformed into resistance spores, were observed intercalary and also in terminal position (Lichtwardt and Moss 1984), while zygospores of A. jatibonicua are formed laterally from an intercalar or terminal cell of the thallus, where the nuclei from the conjugation tube migrate into the sexual spore. The knowledge that zygospores in the new species are not formed directly from the conjugation tube or immediate cells but few cells further is not new within gut fungi. In Harpellales, Farr and Lichtwardt (1967) found zygospore formation far from the conjugation tube in an unidentified Legeriomycetaceae. Migration of nuclei away from the conjugation tube is possible because Asellariales, Harpellales, Kickxellales, Dimargaritales and Zoopagales have characteristic septa with a central plugged pore that allow nuclear circulation (Saikawa 1989, Saikawa et al 1997). The exact process affecting the nuclei of involved cells during zygospore formation in Harpellales is not well understood. Nonetheless TEM images suggest that meiosis occurs after an early plasmogamy and karyogamy between conjugant cells, just before zygospore formation (Moss and Lichtwardt 1977). By this strategy the zygospore ensures fast germination and growth after being consumed by the host (Moss and Lichtwardt 1977, Lichtwardt et al 2001). Within Asellariales the process has not been investigated, and further studies are needed to confirm nuclear phases in both orders.
Harpellales may produce zygospores in particular conditions, that is when compatible thalli are available (heterothallic species) and the host is near molting (hormonal influence) or injured, promoting the development of long-lasting structures in the symbiotic fungi such as thick-walled zygospores to endure in the external environment (Lichtwardt et al 2001). In the case of Asellaria jatibonicua, zygospores were observed within hosts that were nearly ready to molt; in fact the old ectodermic hindgut was detached and probably being expulsed; thalli carrying zygospores had most cells already dead. In Harpellales this situation is typically found in molted hindguts, where zygospores are easier to observe, although thalli are often dead, moribund or damaged, covered with debris and filamentous bacteria.
Asellarian zygospores are remarkable for their morphologic divergence from those of Harpellales. In fact all predictions regarding zygospore morphology in Asellariales pointed to a harpellid type, that is conical or biconical zygospores (Lichtwardt 1973). Within Harpellales zygospores are remarkably constant among different genera, with four types designed according to their position on the corresponding zygosporophore (Moss et al 1975). Related zygomycotans, as Kickxellales, actually considered to be monophyletic with Harpellales and Asellariales (Lichtwardt et al 2001, Tanabe et al 2004, White et al 2006) present spherical hyaline zygospores (Benjamin 1979), similar to Asellarian sexual spores. This resemblance morphologically supports the current conception of Zygomycota systematics. The peculiar septal plugged pore has promoted a "kickxellid clade" supported by molecular data (Tanabe et al 2004, White et al 2006, Hibbett et al 2007). The kickxellid-like zygospores of Asellariales adds morphological support to the close relationship of these orders. Whether the Asellariales are more closely related to the Kickxellales or to the Harpellales could be investigated easily with molecular phylogenies. Unfortunately it has not yet been possible to generate amplified sequences from Asellariales. Asexual spores and thallial features have been responsible of the extended consideration that Harpellales and Asellariales are sister taxa (Benjamin 1979, Moss 1979, Lichtwardt et al 2001). The pattern of arthrospore germination in Asellaria ligiae perfectly resembles the dispersive unit (generative cell plus trichospore) of the Harpellid Carouxella Manier et al 1961 (Lichtwardt 1973). The presence of rounded zygospores does not necessarily contradict this conception. Hydrodynamic Harpellid zygospores are adapted to the aquatic environment where their hosts live, as well as to a rapid germination within the host gut lumen (Lichtwardt 1986). On the other hand, Asellariales likely have a terrestrial origin, although some species inhabit freshwater and marine isopods. If this is the case, we hypothesize that a hydrodynamic morphology of zygospores is not required; moreover a rounded shape would be preferred against a desiccant terrestrial environment, as the superficial area is reduced compared to a conical or biconical shape. Whereas an aquatic or a terrestrial origin of the group can be discussed, the second is more probable, taking into consideration that terrestrial Kickxellales are probably the ancestors of both Harpellales and Asellariales, and the derived character state would be the biconic or conical zygospores secondarily adapted to aquatic environments (White et al 2006, Hibbett et al 2007).
The ectodermic origin of the hindgut and foregut explains its periodic removal together with the rest of ectodermic tissue of the exoskeleton. This molting process affects the fungal symbionts attached to the chitinous hindgut and foregut linings as they have to adapt their development to the molting cycle of the host. In some instances arthropods eat their own molts to recover minerals and proteins (Zimmer 2002). It is common among terrestrial isopods and diplopods (Gere 1956) and is observed easily when isopods are kept in captivity and dissected a day after molting because the content of the gut can be identified as the chitinous exoskeleton. The gut contents of the studied isopods presented obvious debris derived from the exoskeleton; this behavior reinforces infestation and persistence of symbionts within an isopod colony and among colonies in the case of individual intrusion or exuvia consumption by other individuals, thus further spreading the fungal symbiosis. If the exoskeleton is not directly consumed, spores have to endure until eaten, by chance, together with other nutritive debris. In the case of Harpellales and aquatic Asellariales, spores are released freely through the anus into the aquatic environment, where they are entangled in the vegetation or other substrate with nonmotile, sticking appendages, which are present in most trichospores (asexual spores) and zygospores of Harpellales, but not in terrestrial gut-fungi nor in Kickxellales.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 E-mail: mjcafaro{at}uprm.edu 
1 Corresponding author. E-mail: laia.guardia{at}uab.cat
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