Myxozoa in high Arctic: Survey on the central part of Svalbard archipelago

Abstract

Myxosporeans (Myxozoa), microscopic metazoan parasitic organisms, are poorly studied in the Arctic region. Our survey of benthic and pelagic fish (n = 234) collected in Isfjorden (Svalbard, Norway) together with detailed morphological and molecular examination revealed the presence of nine myxosporean species. We compared observed myxosporean diversity with diversity documented in regions close to the Arctic and revealed that water depth rather than geographic distribution is an important factor influencing myxosporean fauna.

We describe three new myxosporean species: Zschokkella siegfriedi n. sp. from kidney of Boreogadus saida, Parvicapsula petuniae n. sp. from the urinary bladder of Gymnocanthus tricuspis, and Sinuolinea arctica n. sp. from the urinary bladder of Myoxocephalus scorpius. We characterise Latyspora-like organism from kidney of Clupea harengus. We provide new data for Ceratomyxa porrecta, Myxidium gadi, Myxidium finnmarchicum, Schulmania aenigmatosa, and Parvicapsula irregularis comb. nov. The phylogenetic analyses including the newly obtained SSU and LSU rDNA data revealed that most of the species studied cluster in the marine urinary clade within the marine myxosporean lineage. Newly obtained sequences including the first molecular data for the member of the genus Schulmania, substantially enriched the Zschokkella subclade. C. porrecta and the two Myxidium species cluster within the Ceratomyxa and marine Myxidium clade, respectively. Newly described species, Z. siegfriedi n. sp., was revealed to be morphologically indistinguishable but genetically diverse from Zschokkella hildae known from numerous gadid fish. Therefore, we consider Z. siegfriedi to be a cryptic myxosporean species that might be misidentified with Z. hildae. A Latyspora-like organism was found to be taxonomically problematic due to its suture line and its distant phylogenetic position from the type species Latyspora scomberomori did not allow us to assign it to the genus Latyspora. Based on an increased taxon sampling and SSU + LSU rDNA-based phylogeny, evolutionary trends within the marine urinary clade are investigated.

Keywords: Arctic; Marine urinary clade; Myxosporea; Phylogeny; Schulmania; Zschokkella.

Graphical abstract

Fig. 1

Mature spores and plasmodia. (A-N) Myxospores and myxosporean plasmodial stages as seen in Nomarski differential interference contrast. Measurements are listed in Table 1. (A) Mature spore of Ceratomyxa porrecta. (B) Spores of Schulmania aenigmatosa with focus on polar capsules (left) and sinuous valve suture (right). (C) Plasmodial stages (left) and mature spore of Parvicapsula irregularis (right). (D) Mature spores of Parvicapsula petuniae. (E) Mature spore of Myxidium gadi. (F) Mature spore of Myxidium finnmarchicum. (G, H) Spores of Sinuolinea arctica in frontal (G) and sutural (H) view. (I, J) Plasmodial stages of Zschokkella siegfriedi. (K) Mature spores of Zschokkella siegfriedi. (L) Plasmodial stage of Latyspora-like organism. (M, N) Latyspora-like organism spores with focus on polar capsules and part of valve suture, respectively.

Fig. 2

Ultrathin section of almost mature spore of Schulmania aenigmatosa with lateral wings (LW) typical for the genus. CC capsulogenic cell, CC with polar capsule (left).

Fig. 3

Histology of Schulmania aenigmatosa infection. (A-C) Schulmania aenigmatosa infection in excretory system of Hippoglossoides platessoides. (A) Early plasmodial stages localised in ureter as seen in histological section stained with HE. (B) Advanced plasmodial stages filling urinary bladder. Giemsa stained stage (inserted). (C) Semithin section stained with toluidine blue documents numerous plasmodial stages attached to the wall of urinary bladder. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Line drawing of Zschokkella siegfriedi, sutural view. Scale bar = 10 μm.

Fig. 5

Histology of Zschokkella siegfriedi infection. (A–C) Zschokkella siegfriedi infection in renal tubules of Boreogadus saida as seen in semithin sections stained with toluidine blue. (A) Infected segment of renal tubule with plasmodial stages in its lumen and densely stained cells in its epithelial lining. (B) Advanced plasmodial stages and amorphous material completely filling the lumen of renal tubule. All epithelial cells are densely stained. (C) Almost mature spores localised in the lumen of renal tubule. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 6

Ultrastructure of Zschokkella siegfriedi infection. (A–C) Details of ultrastructure of Zschokkella siegfriedi as seen in transmission electron microscope. (A) Early developmental stage (EDS) localised within epithelium of renal tubule. Epithelial cells (EC) differ substantially in electron-density due to differences in density of mitochondria. Arrows mark basal membrane of renal tubule, NEC nucleus of epithelial cells, M mitochondria. (B) Almost mature spore in longitudinal section. VC valvogenic cell, NVC nucleus of VC, CC capsulogenic cells, NCC nucleus of CC, S sporoplasm, NS nucleus of S, PPF primordium of polar filament, M mitochondria. C. Valves (V), the polar capsule wall (PCW), and some sections of the polar filament coils.

Fig. 7

Line drawing of Parvicapsula petuniae, sutural view. Scale bar = 10 μm.

Fig. 8

Line drawing of Sinuolinea arctica, sutural view. Scale bar = 10 μm.

Fig. 9

Line drawing of Latyspora-like organism, sutural view. Scale bar = 10 μm.

Fig. 10

The histology of kidney infected with Latyspora-like organism. (A–B) Advanced stage of Latyspora-like organism infection in renal tubules of Clupea harengus. (A) Epithelium in infected segments of renal tubules consisting of cells with pyknotic nuclei suggestive of cellular necrosis. (B) Early stage of epithelial disintegration. (C) Loss of integrity of epithelium due to advanced necrotic changes. Basophilic remnants seen in necrotic epithelium indicate hypertrophy of some nuclei. (D) Hypertrophy of renal corpuscles containing foreign material in Bowman’s spaces was observed but cannot be solely associated with Latyspora-like organism infection.

Fig. 11

Maximum likelihood tree (-ln = 18360.2248) based on 52 SSU rDNA myxosporean sequences available in GenBank and newly obtained data (in bold blue colour) belonging to the marine urinary clade. Numbers at the nodes represent the bootstrap values and the Bayesian posterior probability (ML/MP/BI) gaining more than 50% support (ML and MP) and 0.5 posterior probability (BI), respectively. Bold branches lead to a node with a bootstrap support of ⩾95 and a Bayesian posterior probability of ⩾0.97. Scale bar is given under the tree. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)