Cucumispora dikerogammarin. gen. (Fungi: Microsporidia) infecting the invasive amphipodDikerogammarus villosus: a potential emerging disease in European rivers

Abstract

Dikerogammarus villosus is an invasive amphipod that recently colonized the main rivers of Central and Western Europe. Two frequent microsporidian parasites were previously detected in this species, but their taxonomic status was unclear. Here we present ultrastructural and molecular data indicating that these two parasites are in fact a single microsporidian species. This parasite shares numerous characteristics of Nosema spp. It forms elongate spores (cucumiform), developing in direct contact with host cell cytoplasm; all developmental stages are diplokaryotic and the life cycle is monomorphic with disporoblastic sporogony. Initially this parasite was described as Nosema dikerogammari Ovcharenko and Kurandina 1987. However, phylogenetic analysis based on the complete sequence of SSU rDNA places the parasite outside the genus Nosema and it is therefore ascribed to a new genus Cucumispora. The key features characteristic to this genus are: presence of a very well-developed, umbrella-shape anchoring disk covering the anterior part of polaroplast; arrangement of isofilar polar filament into 6-8 coils convoluted with different angles, voluminous diplokaryon, thin spore wall and relatively small posterior vacuole containing posterosome. The parasite infects most host tissues but mainly muscles. It showed high rates of horizontal trophic transmission and lower rates of vertical transmission.

Microsporidian disease of the invasive amphipod Dikerogammarus villosus and the potential for its transfer to local invertebrate fauna

“…Individuals were then placed in separate pots (10 cL), without food, under the same light and temperature conditions as during acclimatization. Thirty symptomatic (white coloration of the muscles visible through the cuticle, see Ovcharenko et al 2010) and 60 asymptomatic adult animals were taken randomly from the sample. Twice as many asymptomatic individuals were taken because Ovcharenko et al (2010) showed that gammarids at the early stage of infection lack the symptoms.…”

“…Thirty symptomatic (white coloration of the muscles visible through the cuticle, see Ovcharenko et al 2010) and 60 asymptomatic adult animals were taken randomly from the sample. Twice as many asymptomatic individuals were taken because Ovcharenko et al (2010) showed that gammarids at the early stage of infection lack the symptoms. Infectious status was later controlled by a PCR-RFLP diagnostic test (see below).…”

“…Agnew and Koella 1997;Vizoso and Ebert 2005;Slothouber-Galbreath et al 2004). A microsporidian disease has recently been discovered in European rivers associated to the invasive gammarid Dikerogammarus villosus (Crustacea, Amphipoda) (Wattier et al 2007;Ovcharenko et al 2010). Dikerogammarus villosus is one of the most invasive freshwater species, colonising major river systems of Western and Central Europe from its Ponto-Caspian origin Bollache et al 2004;Grabowski et al 2007a;Wattier et al 2007;Bacela et al 2008).…”

“…Due to several favourable life-history traits and to its top predator position in the food chain, D. villosus is able to outnumber rapidly other macroinvertebrate species in colonized areas (Dick and Platvoet 2000;Bollache et al 2004;Van Riel et al 2006;Pöckl 2007;Grabowski et al 2007b). Dikerogammarus villosus is the typical host for the microsporidia Cucumispora dikerogammari (Ovcharenko and Kurandina 1987;Wattier et al 2007, Ovcharenko et al 2010, which spreads out successfully with its host and was identified in many populations all over Europe (Wattier et al 2007). Its prevalence was variable between D. villosus populations, reaching peaks of about 72% prevalence in populations where the host has been established for 3-5 years (Wattier et al 2007).…”

“…Its prevalence was variable between D. villosus populations, reaching peaks of about 72% prevalence in populations where the host has been established for 3-5 years (Wattier et al 2007). This microsporidium is transmitted between individual hosts mainly horizontally, but its presence in ovaries suggests it can occasionally be vertically transmitted (Wattier et al 2007;Ovcharenko et al 2010). Its massive presence in muscles suggests pathogenicity to its host, but no study was dedicated to specifically measure its virulence.…”