Manayunkia occidentalis: A new species of Sabellid Polychaete from the Pacific Northwest of the United States, and an alternate host of two Myxosporean parasites of Salmonid Fish.

Annelids are a diverse and speciose invertebrate group, particularly in marine systems. Apart from Clitellate Annelids ('Oligochaetes' and 'Leaches'), there are relatively few known freshwater species, and several of these belong to the Sabellid genus Manayunkia. Manayunkia currently contains 11 accepted nominal species, though this may need further assessment. The most recent taxa described are the marine Manayunkia mizu, described in 1996 from Papua New Guinea, and the freshwater Manayunkia zenkewitschii, described in 1997 from Lake Baikal. Currently, there are freshwater Manayunkia described from Europe and North America, and brackish/marine species known from Australia, Europe, Papua New Guinea and Brazil. Two species of Manayunkia are recorded from North America: Manayunkia aestuarina, from brackish coastal environments (though the type locality is in the UK), and Manayunkia speciosa, which was first briefly described by Joseph Leidy in 1859, from the Schuylkill River in Pennsylvania, and in much greater detail from specimens from New Jersey in 1883. The species was later reported from the Great Lakes in 1829, the Klamath and Sacramento river basins of Oregon and California in 1966, lakes in Alsaka in 1967, and lakes in North Carolina in 1971. Manayunkia speciosa has been identified as the invertebrate alternate host of two Myxosporean parasites of Salmonid Fish: Ceratonova shasta (formerly Ceratomyxa shasta) and Parvicapsula minibicornis. Myxosporeans are common Myxozoan Cnidarian parasites with complex life cycles that require two hosts: a vertebrate (usually a Fish) in which parasite Myxospores develop, and an invertebrate (usually an Annelid) in which actinospores develop. Both Ceratonova shasta and Parvicapsula minibicornis are widespread in the Pacific Northwest but have not been recorded from the Great Lakes, or east coast of North America, despite presence of both Manayunkia speciosa and susceptible Salmon hosts in these regions.

In a paper published in the journal Zootaxa on 17 March 2020, Stephen Atkinson and Jerri Bartholomew of the Department of Microbiology at Oregon State University, and Greg Rouse of the Scripps Institution of Oceanography at the University of California, San Diego, present the results of a survey based upon the hypothesis that that these two Myxozoans actually require a heretofore unrecognized Annelid host, which is present only in western North American river basins, and which has been consistently mis-identified as Manayunkia speciosa.

Atkinson et al. sampled both infected and uninfected Annelids from the two localities where the parasites were recorded originally from their annelid hosts: the Klamath River, California, and the Willamette River, near Corvallis, Oregon. Using morphology and mitochondrial Cytochrome oxidase subunit I DNA sequencing, they compared these specimens with Manayunkia speciosa samples from New Jersey and the Great Lakes. Atkinson et al. discovered that all Klamath and Willamette Manayunkia, both infected and uninfected, were a novel species, they further sequenced Annelid samples from collections made between 2006 and 2018 and identified only the new species. They did not detect any Manayunkia speciosa from either river basin.

Annelids were collected by hand at depths of 10–50 cm from rocks and periphyton from the Klamath River, California, from below Iron Gate Dam. Additional specimens were collected from the Willamette River, Oregon. Under a dissection microscope, living Annelids were separated from substrate, then examined by light microscopy either alive or fixed in 10% neutral buffered formalin, frozen for DNA analysis, or fixed in 2% glutaraldehyde in cacodylate buffer for electron microscopy. Type and voucher specimens were deposited in the Benthic Invertebrate Collection at Scripps institution of Oceanography, La Jolla, California. To confirm identity and infection status, Atkinson et al. examined additional archived Annelid samples collected opportunistically 2006–2018 by Oregon State University as part of their long term, on-going ecological and disease studies of parasites Ceratonova shasta and Parvicapsula minibicornis. These samples were collected from localities in the Klamath and Willamette Rivers. Atkinson et al. also obtained Manayunkia speciosa from Lake Superior (St. Marys River, Ontario, Canada) and South River, New Jersey, in 2009. A marine Fabriciid, Echinofabricia goodhartzorum, was used as the outgroup, since Echinofabricia has been shown to be the sister group to Manayunkia.

Live Annelids were found in clusters of tubes, most often attached to rocks or intertwined with periphyton. Females were observed frequently with broods of larvae in their tubes. Males and females with overt parasite infections often lacked gametes. Five individuals were sequenced from the type collection locality/date, with an additional 79 from archival material from the Klamath River; 10 were sequenced from the Willamette River. The five paratype specimens were up to 1.6% divergent with each other (0–6 nucleotides differed over the total alignment of 439 nucleotides), compared with a divergence of up to 2.8% among all 84 Klamath River Annelids sequenced. The 10 Willamette River specimens were up to 0.4% divergent with each other, and pairwise distances between Willamette and Klamath River specimens were 3.1–4.1%. These west coast samples were 10.5%–12.2% divergent from the Great Lakes and East Coast Manayunkia speciosa reference sequences. The parasite Ceratonova shasta was detected in 16 Annelids from the Klamath River, whereas Parvicapsula minibicornis was detected in four annelids from the Klamath River and one from the Willamette River; these parasite abundances were typical.

The new species is named Manayunkia occidentalis, which is derived from the Latin word for 'west', to contrast with Manayunkia speciosa, which occurs in eastern and central North American drainages. The holotype (SIO-BIC A12115) is a male with eight thoracic segments and three abdominal segments. Total length (unfixed) 3.0 mm, crown 0.3 mm. Body cylindrical with tapering, dorso-ventrally flattened abdomen. Body wall translucent grey with minor brown pigmentation on peristomium and pygidium, and green pigmentation on chaetiger 6. Branchial crown about 10% of total body length. Two pairs of radioles, each with six pinnules. One ventral pinnule on radiole with 4–5 yellow-white spots in life. One pair of vascularised, unbranched ventral filamentous appendages present, extending for about two-thirds length of radiolar crown, approximately same width as pinnules. Anterior peristomial ring with membranous collar, followed by posterior peristomial ring. Collar margin smooth, higher ventrally, separated by a narrow dorsal gap that corresponds with ciliated faecal groove. Peristomial eyes, black rounded spots. Pygidial eyes absent. Superior thoracic notochaetae elongate, narrowly hooded; 5–7 per fascicle (chaetigers 1–5), 4–5 per fascicle (chaetigers 6–8). Inferior thoracic notochaetae on chaetigers 1–8 short; 3–4 per fascicle except chaetiger 2, which has 6 per fascicle. Thoracic neuropodia each with 4–7 uncini in chaetigers 2–8. Thoracic uncini with rows of evenly small teeth gradually decreasing in size away from main fang. Position of chaetae and uncini reversed in abdominal segments; number of abdominal uncini per fascicle decreasing posteriorly from 22 to 9. Abdominal uncini each with multiple rows of teeth that are uniform in size; manubrium at least five times longer than dentate region, with base about two thirds the width of the dentate region. Abdominal neuropodia are elongate, narrowly hooded, decreasing posteriorly from 4–6 to 2 per fascicle.

 

Gross morphological features of Manayunkia occidentalis resolved by light microscopy: (A) multiple individuals emerged and feeding from their tubes; (B) Individual annelid with prominent vascularized appendages (va) and showing refractile spots on one feeding palp on each side (arrowheads); (C) female in reflected light, showing white oocytes (o) in segments 4–6; (D) male in reflected light showing bright spermatogonic tissue (sp) in multiple posterior segments; (E) Male in transmitted light showing parallel vascularized appendages (va) and fanned-out feeding palps nteriorly with two dark eyespots in peristomium, and granular coelom posteriorly due to presence of developing sperm. Atkinson et al. (2020).

Paratypes are similar to the holotype. However, females have oocytes in thoracic chaetigers 4–5 and a pair of pigmented spermathecae in the base of the radiolar crown. Females differ from males in having thoracic neuropodia with uncini in chaetigers 2–5 followed by 3–6 elongate hooded chaetae in neuropodia of chaetigers 6–8. 

 

Images showing chaetal characters of Manayunkia occidentalis: (A) inferior and superior notochaete typical of thoracic segments 2–8; (B) thoracic uncini; (C) abdominal uncini; (D) dorsal view of posterior thoracic segments and abdomen of male showing typical uncini in chaetigers t7 and t8 (arrowheads) and in scanning electron micrograph shown in (F); (E) dorsal view of posterior thoracic segments and abdomen of female showing neuropodia of thoracic chaetigers 6–8 with elongate neuropodia instead of uncini, seen also in scanning electron micrograph in (G) (arrowhead). (H) anterior thoracic segment of female showing notochaetae and uncini (arrowhead), characteristic of thoracic segments 2–5 in both sexes. Atkinson et al. (2020).

Manayunkia speciosa was described originally from Philadelphia, USA with subsequent reports from the Great Lakes and several west coast river basins. This Annelid is reported to be the obligate alternate host of two Myxozoan parasites Ceratonova shasta and Parvicapsula minibicornis. Unambiguous identification of the invertebrate hosts of Myxozoans, which produce the infectious stage to Fish, is essential for risk assessment and stock management as these parasites cause disease and death within populations of salmon and trout. Atkinson et al.'s findings support the hypothesis that the Annelid host of the parasites has likely been mis-identified as Manayunkia speciosa, and is actually a novel taxon Manayunkia occidentalis.

 

Morphological features of Manayunkia occidentalis resolved by scanning electron microscopy: (A) lateral view; (B) dorsal view; (C) ventral view; (D) anterior showing membranous collar (c) of the peristomal ring (pr), margin with fecal groove (fg); mucus covers the pinnules and adheres Diatoms; (E) detail of typical thoracic uncini; (F) abdominal segments and anus, showing ciliated fecal groove extending anteriorly and wrapping around to the ventral surface at boundary between abdominal and thoracic segments; (G) lateral view of thoracic segments showing contracted uncini and prominent neuropodia; (H) higher magnification view of retracted abdominal uncini. Atkinson et al. (2020).

The 94 west coast Manayunkia occidentalis specimens that Atkinson et al. characterised had cytochrome oxidase subunit I sequences at least 11% different from the reference Manayunkia speciosa sequences from Lake Superior and New Jersey. This east-west genetic divergence underpinned the rationale for describing the west coast Annelids as a distinct, novel taxon. Among the Manayunkia occidentalis specimens, the greatest genetic difference (4.1%) was between isolates from the two rivers, which are more than 500 km apart. These genetic differences are not surprising given the relative immobility of the Annelids, particularly from above- and below-dam localities, and between river basins separated by saltwater. Atkinson et al. hypothesise that similar degrees of genetic differences, with corresponding novel haplotypes, will be observed among populations in other unconnected river basins on the West Coast (Fraser, Rogue, Sacramento), and probably within large basins like the Columbia.

Atkinson et al. did not detect any Manayunkia speciosa among the 94 Annelids sampled from multiple localities in two river basins. This was surprising given historical records of that taxon in West Coast basins, particularly associated with Myxozoan parasites. The collection localities in the Klamath River included one where 'Manayunkia speciosa' was collected and sequenced previously. This published sequence is only minimally divergent (0–1%) from Manayunkia speciosa reference sequences collected from Lake Superior and the East Coast. Atkinson et al. cannot explain how these trans-continental Manayunkia speciosa sequences could be so similar, given that they observed genetic distances up to 2.8% among Manayunkia occidentalis samples from the Klamath Basin, and up to 4.1% between specimens from different West Coast river basins. Based on their survey data, Atkinson et al. postulate that Manayunkia speciosa may not be present in the Klamath or Willamette rivers, and they suspect that the earlier assignations of Klamath River Annelids as Manayunkia speciosa are incorrect. Almost all previous identifications relied on morphology, and Atkinson et al. have now shown that there are few morphological characters to distinguish the two taxa, though the markedly smaller number of pinnules in Manayunkia occidentalis is an obvious difference from Manayunkia speciosa. This and the cytochrome oxidase subunit I sequence divergence of at least 10.5% makes future discrimination between Manayunkia speciosa and Manayunkia occidentalis relatively straightforward.

Twenty-one of the 94 examined annelids were infected with either or both Ceratonova shasta and Parvicapsula minibicornis, and all were identified by sequence as Manayunkia occidentalis, and thus Atkinson et al. could not confirm that Manayunkia speciosa is a host for these Myxozoans. If Manayunkia speciosa is not a permissive host, then this would explain why Ceratonova shasta and Parvicapsula minibicornis have not become established in the Great Lakes or in East Coast river systems where Manayunkia speciosa, only, is present. It is likely, however, that Manayunkia speciosa hosts other Myxozoan species, as evidenced by detection of Ceratonova-like DNA in Annelids from the Great Lakes. Atkinson et al. predict that they will find Manayunkia occidentalis in all river basins where the parasite is found on the west coast, and none in the Great Lakes. Accordingly, they are sampling and sequencing additional Annelid populations from river basins where Ceratonova shasta and Parvicapsula minibicornis occur, to determine the phylogeography of the host, any correlation between infection and host haplotype, and if any Manayunkia speciosa sensu stricto exists on the west coast of North America.

See also...

Follow Sciency Thoughts on Facebook.

 

Discovering the origins of Myxozoan parasites.

Myxozoans are parasitic Euaryotic organisms that typically have a two host life-cycle. In most forms this involves a stage which infects an invertebrate, often an Annelid Worm, and a stage which infects a vertebrate host, usually a Bony Fish. For example the Myxozoan Myxobolus cerebralis infects Tubifax Worms, Tubifex tubifex, producing a large number of infective actinospores which are capable of anchoring onto Rainbow Trout, Oncorhynchus mykiss. Once attached to a Trout host the actinospore injects its protoplasm into the host's tissue, where a second life-cycle stage develops, the Myxospore, incidentally causing Whirling Disease in the Fish (a disease that causes both deformation of the spine and neurological damage in growing Fish, causing them to 'whirl' when they attempt to swim). These myxospores are released into the water when the Fish dies (usually prematurely) and are eventually consumed by new Tubifex Worm hosts, and the cycle repeats itself.

Myxozoans were first discovered in the 1880s, and were assumed to be Protists, single-celled Eukaryotes such as Amoebae, though some species have been shown to produce multicellular stages as part of their life-cycle, for example some Malacosporean Myxozoans produce a vermiform ('worm-like') stage. However since the 1990s several genetic studies have suggested that Myxozoans might be descended from multi-cellular animals, with different studies recovering them as either members of the Cnidaria (the group that includes Jellyfish, Corals and Sea Anemones) or as the sister-group to the Bilateria (all animals except Cnidarisns, Sponges and Ctenophores – Sea Combs). This is not totally surprising, as parasites often show very reduced body-plans, losing the ability to perform functions they rely on their hosts to do as part of an evolutionary drive to reduce their body-size. Myxozoans also produce some proteins otherwise only known in Cnidarians, and the polar capsule used by the actinospore stage Myxozan to inject its protoplasm into a vertebrate host has been compared to the nematocysts (stinging cells) of Cnidarians, further supporting the idea that Myxoans and Cnidarians may be closely related.

In a paper published in the Proceedings of the National Academy of Sciences of the UnitedStates of America on 16 November 2015, Sally Chang of the Departmentof Ecology and Evolutionary Biology at the University of Kansas, Moran Neuhof of the Department of Zoology and Department ofNeurobiology at Tel-Aviv University, Nimrod Rubinstein of the Department of Molecular and Cellular Biology at Harvard University, Arik Diamant of the National Center for Mariculture at Israel Oceanographic and Limnological Research, Hervé Philippe of the Station d’Ecologie Expérimentale du Centre national de la recherche scientifique and the Département de Biochimie at the Université de Montréal, Dorothée Huchon, also of the Department of Zoology at Tel-Aviv University and PaulynCartwright, also of the Department of Ecology and Evolutionary Biology at the University of Kansas, describe a genetic phylogeny of the Myxozoa and Cnidaria developed using the complete genomes of two distantly related Myxozoans, Kudoa iwatai and Myxobolus cerebralis, plus the previously published genomes of three other Myxozoan species, Buddenbrockia plumatellae, Tetracapsuloides bryosalmonae, and Thelohanellus kitauei, as well as 23 species of Cnidarians and 38 representatives of other animal groups, plus nine unicellular Eukaryotes.

Myxobolus cerebralis alternates its development between a Fish (Salmonid) host and an Annelid (Tubifesx tubifex) host. The myxospore is produced in the Fish (Right), and the actinospore is produced in the Annelid (Left). Both stages consist of just a few cells, including those housing polar capsules. Chang et al. (2015).

Chang et al. paid particular attention to one particular Cnidarian, Polypodium hydriforme, which is highly unusual in that, like Myxoans, it is parasitic. Polypodium hydriforme has a two stage life-cycle, with a free living stage that resembles a small Jellyfish and a parasitic stage that infects the oocytes (unfertilized eggs) of Paddlefish and Sturgeon. This parasitic stage of Polypodium hydriforme resembles the stolon of Jellyfish, an attached Hydroid-like stage which hatches from eggs produced by the free-swimming Medusa stage Jellyfish. The stolon of Jellyfish grows attached to a substrate then divides asexually into numerous new Medusae, while that of Polypodium hydriforme develops within the oocytes of the Fish, then fragments into numerous new adults.

In Polypodium hydriforme, the stolon stage (Top) develops inside the ovaries of its host (Acipenceriform fish). Upon host spawning, Polypodium hydriforme emerges from the host’s oocyte (Right), fragments, and lives as a free-living stage with a mouth (Left) before infecting its host. Chang et al. (2015).

Previous studies of Cnidarian phylogeny have suggested that Polypodium hydriforme is a sister-group to the Medusozoa (Jellyfish), i.e. all Jellyfish share a common ancestor more recent than their last shared ancestor with Polypodium hydriforme, but that that shared ancestor lived more recently than the common ancestor of the Medusozoa and any other known Cnidarian group.

Chang et al.'s findings support the close relationship of Polypodium hydriforme and the Medusazoa, but place the Myxozoa within the Cnidaria as the sister-group to Polypodium hydriforme; i.e. the most recent common ancestor of all known Myxozoans lived more recently than the common ancestor of Myxozoans and Polypodium hydriforme, and that shared ancestor had a shared ancestor with the Medusazoa more recently than with any other Cnidarian group.

Phylogenetic tree generated from a matrix of 51,940 amino acid positions and 77 taxa using Bayesian inference under the CAT model. Support values are indicated only for nodes that did not received maximal support. Bayesian posterior probabilities/ML bootstrap supports under the PROTGAMMAGTR model are given near the corresponding node. A minus sign (‘‘−’’) indicates that the corresponding node is absent from the ML bootstrap consensus tree. Chang et al. (2015).

This analysis supports the idea that the Myxozoans are Cnidarians, but it also implies on some very long gaps in the evolutionary record, and such gaps can be problematic; when looking at the relationships between distantly related groups without intervening taxa the limited amount of data can be misleading, resulting in false conclusions.

To try to overcome this problem Chang et al. next looked at the surviving genes in the Myxozoans examined. Just as the morphology of parasites is often greatly simplified, so they tend to lose much of their genetic heritage, with genes and gene-families which code for functions no longer performed by the parasite. Myxozoans have genomes comparable with the simplest other animal genomes yet described, those of parasitic Nematodes. Chang et al. found that Myxozoans have lost most of the genes used for body patterning, cellular differentiation and intercellular communication, though these are still present in Polypodium hydriforme, but other gene-families, such as those involved in stem-cell differentiation were still present, and showed clear affinities to those of other Cnidarians.

See also...

Cryptosporidium discovery at water treatment plant leaves around 300 000 without drinkable water in Lancashire, England.                                                        Around 300 000 homes were left without drinkable...

An enigmatic animal from the Australian continental shelf, with possible similarities to some members of the Ediacaran Fauna.         The Ediacaran Fauna comprises a group of fossils...

A possible Cnidarian from the Late Ediacaran of Newfoundland.                                           The fossils of the Ediacaran Period record the first widespread macrofossils in the rock-record. Many of these fossils do not appear to belong to any modern group, but instead are thought to belong to an extinct taxa (sometimes known as ‘Vendobionts’), which may-or-may-not be related to modern Animals, though some fossils have been linked to Sponges (a group which...

Follow Sciency Thoughts on Facebook.