An Isonema-like flagellate (Protozoa: Mastigophora) infection in larval geoduck clams, Panope abrupta

doi:10.1016/0022-2011(87)90086-3

Journal of Invertebrate Pathology

Volume 50, Issue 3, November 1987, Pages 221-229

https://doi.org/10.1016/0022-2011(87)90086-3 Get rights and content

Abstract

Cultured geoduck clam (Panope abrupta) larvae were naturally infected with an Isonema-like flagellate. Free-swimming larval clams were initially infected by flagellates that penetrated the mantle and proliferated within the coelom. Larvae with heavy infections accumulated on the tank bottoms and ultimately died. The protozoan was identified as an Isonema-like flagellate based primarily on the presence of a distinctive ingestion apparatus composed of a microtubule complex, the presence of large, peripherally oriented mitochondria with sparse cristae, subplasmalemmal microtubules, the lack of a pellicle, short flagella, and pronounced metaboly. This is the first report of an invasive, pathogenic Isonema and the first report of a protozoan disease of a larval bivalve mollusc.

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Cited by (28)

Diplonemids – A Review on “New” Flagellates on the Oceanic Block
2022, Protist
Citation Excerpt :
Other Rhynchopus spp. were reported in association with marine animals as parasites or commensals, as in the case of a lobster infected with a parasitic dinoflagellate Hematodinium sp., where diplonemids were observed in blood and on the gills (von der Heyden et al. 2004). Similarly, diplonemids were a part of a large microbial community on the gills of a marine crab (Bodammer and Sawyer 1981) or were directly implicated with pathogenesis observed in cultured marine clams (Kent et al. 1987). Several Diplonemidae have been observed in association with aquatic plants.
Diplonemids are a group of flagellate protists, that belong to the phylum Euglenozoa alongside euglenids, symbiontids and kinetoplastids. They primarily inhabit marine environments, though are also found in freshwater lakes. Diplonemids have been considered as rare and unimportant eukaryotes for over a century, with only a handful of species described until recently. However, thanks to their unprecedented diversity and abundance in the world oceans, diplonemids now attract increased attention. Recent improvements in isolation and cultivation have enabled characterization of several new genera, warranting a re-examination of all available knowledge gathered so far. Here we summarize available data on diplonemids, focusing on the recent advances in the fields of diversity, ecology, genomics, metabolism, and endosymbionts. We illustrate the life stages of cultivated genera, and summarise all reported interspecies associations, which in turn suggest lifestyles of predation and parasitism. This review also includes the latest classification of diplonemids, with a taxonomic revision of the genus Diplonema. Ongoing efforts to sequence various diplonemids suggest the presence of large and complex genomes, which correlate with the metabolic versatility observed in the model species Paradiplonema papillatum. Finally, we highlight its successful transformation into one of few genetically tractable marine protists.
Hemocyte cell types of the Cortes Geoduck, Panopea globosa (Dall 1898), from the Gulf of California, Mexico
2020, Fish and Shellfish Immunology
Citation Excerpt :
It is known that the movement of shellfish stocks favours dispersion of diseases of aquatic animals with negative potential impact for fishery and aquaculture practices, and baseline information about symbionts, parasites, anatomy and histology of geoduck clam tissues is needed to study potential negative impacts of biotic and abiotic factors on the clam's health [5,6]. Several symbionts and parasites have been recorded in apparently healthy adult wild or cultured geoduck clams since the only signs of anomalies (unhealthy appearance) known to date are the presence of warts, blisters or scars on the siphon and the mantle between the shells as well as pustules or black/brown colouration (dark leathery surface of geoduck clams) probably caused by fungus in the same tissues [5–12]. However, none of the etiological agents associated with these lesions have been identified.
The geoduck Panopea globosa is an endemic and economic valuable species from the Mexican Northwest coast whose biology has been little studied. No information exists about their hemocytes to date, which is highly important to assess the welfare of wild and cultured organisms. In this study, hemocytes of adult P. globosa were characterized at the morphological, ultrastructural and functional level. The mean number of hemocytes in the hemolymph of P. globosa was 6 × 10⁵ ± 2 × 10⁵ cells mL⁻¹. The cells were identified as granulocytes (Gr) and hyalinocytes (H). The former accounted for 28% of adhered cells in the hemolymph, measured 6–18 μm, showed numerous basophilic granules in the cytoplasm, with round and eccentric nuclei, and a nucleus:cytoplasm ratio of 0.44 ± 0.01. Hyalinocytes were the most abundant cells in the hemolymph of P. globosa (72% adhered cells) and were subdivided, according to their size, in small (Hs) 4–12 μm and large (HL) 6–18 μm. Hyalinocytes were eosinophilic round or ovoid cells with a central or eccentric nucleus, few or no granules in the cytoplasm and similar nucleus:cytoplasm ratio (Hs: 0.63 and HL: 061). Lysosomes and lipids were observed in Gr, while carbohydrates were the most abundant energy substrate in H. Both hemocytic cell types, mainly Gr, were capable to ingest particles and yield superoxide (P > 0.05). The present study shows for the first time the cell types, abundance and immune activities of hemocytes present in the hemolymph of P. globosa. This information provides a useful baseline to carry out further research on the cellular immune response of the clam to potential pathogens or changes in environmental factors.
Allobodo chlorophagus n. gen. n. sp., a Kinetoplastid that Infiltrates and Feeds on the Invasive Alga Codium fragile
2018, Protist
Citation Excerpt :
Other parasitic/commensal groups include Ichthyobodo, species of which are obligate ectoparasites of fish, Trypanoplasma (and Cryptobia proto parte), which infect fish and leeches, ‘true’ Cryptobia from snails and fish, Jarrellia from whale blowhole mucus, Cruzella, which was originally isolated from tunicates, and Azumiobodo, which also infects tunicates, causing soft tunic syndrome (Hirose et al. 2012; Kim et al. 2013; Kumagai et al. 2011; Noga 2010; Poynton et al. 2001; Todal et al. 2004; Vickerman 1990, 2000; Woo 2003). Furthermore, the sister group to Kinetoplastea, diplonemids (Diplonemea), is suspected to contain a range of parasitic/parasitoid taxa based on direct observation or indirect inference (e.g. Flegontova et al. 2016; Kent et al. 1987; von der Heyden et al. 2004). In particular, some diplonemids infiltrate through the cell walls of larger unicellular algae, specifically diatoms, then feed and replicate (Elbrächter et al. 1996; Schnepf 1994; Yabuki and Tame 2015).
A novel biflagellate protist that consumed chloroplasts inside material of the invasive marine green alga Codium fragile was reported from the U.S. east coast in 2003. We observed a similar association in C. fragile from five sites in Nova Scotia, Canada during 2013 and 2014. After incubating Codium fragments for 2–3 days, some utricles and filaments contained numerous chloroplast-consuming cells. Transmission electron microscopy (TEM) confirmed that these were kinetoplastids with a pankinetoplast, large electron-dense droplets in the cytoplasm and a connective between the paraxonemal rod bases, but no conspicuous para-cytopharyngeal rod, all consistent with U.S. material observed in 2003. The ITS1-5.8S rRNA-ITS2 sequences from 13 Nova Scotia isolates were identical. SSU rRNA gene phylogenies placed the Codium-associated kinetoplastid in neobodonid clade ‘1E’. Clade 1E likely contains no previously described species, and branches outside all other major neobodonid groups, either as their sister or as a separate lineage, depending on rooting. These results indicate that the kinetoplastid represents a single species that merits a new genus (and family), and we describe it as Allobodo chlorophagus n. gen., n. sp. The lack of evidence for food sources other than Codium is consistent with a parasitic association, but other possibilities exist (e.g. necrotrophy).
Phylogeny and Morphology of New Diplonemids from Japan
2018, Protist
Citation Excerpt :
It seems that parasitism, at least transient, as well as predation, are common life strategies for members of the genus Rhynchopus. Indeed, several species were found to parasitize crabs, lobsters and clams (Bodammer and Sawyer 1981; Kent et al. 1987; von der Heyden et al. 2004), while R. coscinodiscivorus predates/parasitizes on diatoms by invading the frustule (Schnepf 1994). So far, the literature refers to diplonemids mostly as to parasites or epibionts of plants and invertebrates or as predators of algae rather than bacterivores or detritus feeders (Vickerman 2000).
Diplonemids were recently found to be the most species-rich group of marine planktonic protists. Based on phylogenetic analysis of 18S rRNA gene sequences and morphological observations, we report the description of new members of the genus Rhynchopus – R. humris sp. n. and R. serpens sp. n., and the establishment of two new genera – Lacrimia gen. n. and Sulcionema gen. n., represented by L. lanifica sp. n. and S. specki sp. n., respectively. In addition, we describe the organism formerly designated as Diplonema sp. 2 (ATCC 50224) as Flectonema neradi gen. n., sp. n. The newly described diplonemids share a common set of traits. Cells are sac-like but variable in shape and size, highly metabolic, and surrounded by a naked cell membrane, which is supported by a tightly packed corset of microtubules. They carry a single highly reticulated peripheral mitochondrion containing a large amount of mitochondrial DNA, with lamellar cristae. The cytopharyngeal complex and flagellar pocket are contiguous and have separate openings. Two parallel flagella are inserted sub-apically into a pronounced flagellar pocket. Rhynchopus species have their flagella concealed in trophic stages and fully developed in swimming stages, while they permanently protrude in all other known diplonemid species.
Unusual Mitochondrial Genome Structures throughout the Euglenozoa
2007, Protist
Mitochondrial DNA of Kinetoplastea is composed of different chromosomes, the maxicircle (bearing ‘regular’ genes) and numerous minicircles (specifying guide RNAs involved in RNA editing). In trypanosomes [Kinetoplastea], DNA circles are compacted into a single dense body, the kinetoplast. This report addresses the question whether multi-chromosome mitochondrial genomes and compacted chromosome organization are restricted to Kinetoplastea or rather occur throughout Euglenozoa, i.e., Kinetoplastea, Euglenida and Diplonemea. To this end, we investigated the diplonemid Rhynchopus euleeides and the euglenids Petalomonas cantuscygni, Peranema trichophorum and Entosiphon sulcatum, using light and electron microscopy and molecular techniques. Our findings together with previously published data show that multi-chromosome mitochondrial genomes prevail across Euglenozoa, while kinetoplast-like mtDNA packaging is confined to trypanosomes.
Protein phylogenies robustly resolve the deep-level relationships within Euglenozoa
2004, Molecular Phylogenetics and Evolution
The deepest-level relationships amongst Euglenozoa remain poorly resolved, despite a rich history of morphological examination and numerous molecular phylogenetic studies of small subunit ribosomal RNA (SSU rRNA) data. We address this question using two nuclear-encoded proteins, the cytosolic isoforms of heat shock protein 90 (hsp90) and heat shock protein 70 (hsp70). For both proteins we examined sequences from the three primary groups within Euglenozoa (euglenids, diplonemids, and kinetoplastids), and from their close relatives, Heterolobosea. Maximum likelihood (ML) and ML distance analyses of these proteins support a close relationship between diplonemids and kinetoplastids to the exclusion of the euglenid Euglena gracilis. In hsp90 and combined protein analyses bootstrap support is very strong and alternative topologies are generally rejected by ‘approximately unbiased’ (AU) tests. This result is consistent with recent molecular biological and morphological data, but contradicts early structural accounts and many SSU rRNA analyses that favour a closer relationship between diplonemids and euglenids. However, a re-examination of an important SSU rRNA data set highlights the instability of the inferences from this marker. The protein analyses also suggest that bodonids are paraphyletic, with trypanosomatids grouping with ‘clade 2’ and ‘clade 3’ bodonids to the exclusion of ‘clade 1’ bodonids.

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Journal of Invertebrate Pathology

Abstract

References (12)

Metamorphosis of the marine gastropod, Phestilla sibogae Bergh (Nudibranchia: Aeolidolea). I. Light and electron microscopic analysis of larval and metamorphic stages

J. Exp. Mar. Biol. Ecol

Diagnosis of vibriosis in a commercial oyster hatchery epizootic: diagnostic tools and management features

Aquaculture

A Rickettsiales-like infection in the Pacific razor clam, Siliqua patula

J. Invertebr. Pathol

Pathology, management and diagnosis of oyster velar virus disease (OVVD)

Aquaculture

Aufwuchs protozoa and bacteria on the gills of the rock crab, Cancer irroratus Say: A survey by light and electron microscopy

J. Protozool

A fungus disease in clam and oyster larvae

Science

Cited by (28)

Diplonemids – A Review on “New” Flagellates on the Oceanic Block

Hemocyte cell types of the Cortes Geoduck, Panopea globosa (Dall 1898), from the Gulf of California, Mexico

Allobodo chlorophagus n. gen. n. sp., a Kinetoplastid that Infiltrates and Feeds on the Invasive Alga Codium fragile

Phylogeny and Morphology of New Diplonemids from Japan

Unusual Mitochondrial Genome Structures throughout the Euglenozoa

Protein phylogenies robustly resolve the deep-level relationships within Euglenozoa

Regular articleAn Isonema-like flagellate (Protozoa: Mastigophora) infection in larval geoduck clams, Panope abrupta

Abstract

J. Exp. Mar. Biol. Ecol

Aquaculture

J. Invertebr. Pathol

Aquaculture

Aufwuchs protozoa and bacteria on the gills of the rock crab, Cancer irroratus Say: A survey by light and electron microscopy

J. Protozool

A fungus disease in clam and oyster larvae

Science

Regular article
An Isonema-like flagellate (Protozoa: Mastigophora) infection in larval geoduck clams, Panope abrupta