Effect of multiple microsporidian infections and temperature stress on the heat shock protein 70 (hsp70) response of the amphipod Gammarus pulex

Grabner, Daniel; Schertzinger, Gerhard; Sures, Bernd

doi:10.1186/1756-3305-7-170

Cited by 24 publications

(23 citation statements)

References 41 publications

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“…505 and 515). The same microsporidians were previously detected in different amphipod species (Terry et al ., ; Krebes et al ., ; Grabner, Schertzinger & Sures, ; Grabner et al ., ; Weigand et al ., ), and can be considered amphipod specific. The only unique host–parasite association was found between the mayfly E. danica and the group D‐ Microsporidium .…”

Section: Discussionmentioning

confidence: 99%

Hidden diversity: parasites of stream arthropods

Grabner

2016

Freshwater Biology

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Summary Parasite communities of aquatic macroinvertebrates have so far rarely been studied, even if these host organisms are of high relevance for the ecology of freshwater systems and their parasites likely affect the host populations and communities. Therefore, this study addresses this ‘hidden diversity’ in aquatic arthropods of a stream ecosystem in North Rhine‐Westphalia, Germany. Samples of benthic organisms were taken, and the most abundant host species of major invertebrate groups (amphipods and larvae of chironomids, beetles, caddisflies, mayflies, stoneflies) were tested by PCR for different parasite taxa [microsporidians, acanthocephalans (only amphipods), trematodes, nematodes]. Furthermore, the possible link between prevalence and host feeding type was investigated for each parasite group using a newly developed ‘feeding type score’. In total, 10 species of aquatic insect larvae and two amphipods of the genus Gammarus spp. were tested and 16 different isolates of microsporidians, three acanthocephalan species, six species of trematodes and one nematode were found. Microsporidians were present in all host species with prevalences ranging from 20 to 100%. Only one presumably specific host–microsporidian association was found for the mayfly Ephemera danica and three isolates were detected exclusively in amphipods. Three acanthocephalan species were detected in the amphipods with prevalences of up to 5.3%. All tested host species were infected with trematodes (prevalences 25–100%), except the caddisfly Sericostoma sp. Nematodes were detected in five host species with prevalences ranging from 14 to 80%. For several positive samples, no sequencing result could be obtained, especially for trematodes and nematodes, therefore, the actual parasite diversity might be even higher. Active filter feeding showed the highest feeding type prevalence score for microsporidia and nematodes, and passive filter feeders for trematodes, but these results have to be interpreted cautiously as only one active and one passive filter feeder species each were present in the sample. The impressive number of 26 parasite species (12 microsporidians and 10 helminths) were detected in 12 host species, mostly with surprisingly high prevalences. These results illustrate the ‘hidden diversity’ in aquatic ecosystems and highlight the importance of parasites for aquatic ecological research and the need for studies on the effects of mixed parasite infections on the host populations and communities.

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Section: Discussionmentioning

confidence: 99%

Hidden diversity: parasites of stream arthropods

Grabner

2016

Freshwater Biology

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“…Their transmission can be horizontal from one individual to another and/or vertical, directly from mother to offspring (Dunn & Smith, 2001). High prevalences and co-infection cases with up to three microsporidian species underline the importance of these parasites for amphipods (Haine et al, 2004;Grabner, Schertzinger & Sures, 2014;Grabner et al 2015). Due to intense proliferation of sporogonic stages microsporidians can modulate the host metabolism or its hormone homeostasis leading to feminization of male individuals (Bandi et al, 2001;MacNeil et al, 2003a;Smith, 2009).…”

Section: Manuscript To Be Reviewedmentioning

confidence: 99%

“…Parasites are natural and ubiquitous parts of ecosystems and their role for ecosystem function and stability has been recognized in recent years (Marcogliese, 2005;Hudson, Dobson & Lafferty, 2006; Kuris et al, 2008). Nevertheless, parasites are often neglected in ecotoxicological research, although results of recent studies showed that they may influence the host response to pollution (Sures, 2004(Sures, , 2008aMarcogliese & Giamberini, 2013) and can impact the stress response of their host, especially on the biochemical level (Sures, Lutz & Kloas, 2006;Sures & Radszuweit, 2007;Frank et al, 2011Frank et al, , 2013Gismondi, Cossu-Leguille & Beisel, 2012a;Gismondi et al, 2012a,b;Filipović Marijić, Vardić Smrzlić & Raspor, 2013;Grabner, Schertzinger & Sures, 2014).…”

Section: Introductionmentioning

confidence: 99%

Peer Review #2 of "Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum (v0.2)"

Short¹

2015

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Amphipods are commonly parasitized by acanthocephalans and microsporidians and coinfections are found frequently. Both groups of parasites are known to have severe effects on their host. For example, microsporidians can modify host sex ratio and acanthocephalans can manipulate the behavior of the amphipod to promote transmission to the final host. These effects influence host metabolism in general and will also affect the ability of amphipods to cope with additional stressors such as environmental pollution, e.g. by toxic metals. Here we tested the effects of sub-lethal concentrations of cadmium on glycogen and lipid levels, as well as on the 70kDa heat shock protein (hsp70) response of field collected Gammarus fossarum, which were naturally infected with microsporidians and the acanthocephalan Polymorphus minutus. Infected and uninfected G. fossarum were exposed to a nominal Cd concentration of 4µg/L, which resembled measured aqueous Cd concentration of 2.9 µg/L cadmium in reconstituted water for 7 d at 15° C in parallel to an unexposed control. After exposure gammarids were snap frozen, weighed, sexed and tested for microsporidian infection by PCR. Only individuals containing the microsporidian Dictyocoela duebenum were used for the further biochemical and metal analyses. P. minutus infected amphipods were significantly smaller than their uninfected conspecifics. Mortality was insignificantly increased due to cadmium exposure, but not due to parasite infection. Microsporidian infection in combination with cadmium exposure led to increased glycogen levels in female gammarids. An increase of glycogen was also found due to interaction of acanthocephalan and microsporidian infection. Elevated lipid levels were observed in all groups infected with microsporidians, while acanthocephalans had the opposite effect. A positive correlation of lipid and glycogen levels was observed. The general stress response measured in form of hsp70 was significantly increased in microsporidian infected gammarids exposed to cadmium. P. minutus did not affect the stress response of its host. Lipid levels were correlated negatively with hsp70 response, and indicated a possible increased stress susceptibility of individuals with depleted energy reserves. The results of our study clearly demonstrate the importance of parasitic infections, especially of microsporidians, for ecotoxicological research.

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“…They are important in many cellular processes, including development, growth, protein folding, signal transduction and apoptosis. They play key roles in response to stress conditions such as thermal stress, parasite infections and heavymetal exposure, and protect organisms against environmentally induced cellular damage (Devaney, 2006;Grabner et al, 2014). Inhibitors of Hsp90 and Hsp70 were investigated as targets for treatment of cancer and parasitic diseases (Edkins and Blatch, 2012).…”

Section: Introductionmentioning

confidence: 99%