Wide geographic distribution of overlooked parasites: Rare Microsporidia in Gammarus balcanicus, a species complex with a high rate of endemism

Abstract

Parasites and other symbionts deeply influence host organisms, and no living organism can be considered to have evolved independent of its symbionts. The first step towards understanding symbiotic influences upon host organisms is a strong supporting knowledge of parasite/symbiont diversity. Parasites of freshwater amphipods are diverse, with Microsporidia being a major group. These intracellular parasites impact gammarid fitness in different ways, ranging from reduced fitness to increased fecundity. Many Microsporidia have been recorded using molecular data, with multiple taxa pending formal taxonomic description. While some parasites are common, others are known only through sporadic records of single infections. In this study, we focus on rare/sporadic microsporidian infections within Gammarus balcanicus , a host species complex with a high level of endemism. In addition to enriching our knowledge on Microsporidia parasite diversity in amphipod hosts, we test whether these symbionts are specific to G. balcanicus or if they are the same taxa infecting other gammarid species. Of 2231 hosts from 87 sites, we catalogued 29 sequences of “rare” Microsporidia clustering into 19 haplogroups. These haplogroups cluster into 11 lineages: four pre-described taxa ( Cucumispora roeselum , C. ornata, C. dikerogammari and Enterocytospora artemiae ) and seven ‘Molecular Operational Taxonomic Units’, which are known from previously published studies to infect other European amphipod species. Our study significantly widens the geographic range of these Microsporidia and expands the known spectrum of hosts infected. Our results suggest that these parasites are ancient infections of European gammarids. For some host-parasite systems, we hypothesize that the common parasite ancestors that infected the hosts' common ancestors, diversified alongside host diversification. For others, we observe Microsporidia taxa with wide host ranges that do not follow host phylogeny.

Generalist parasites persist in degraded environments: a lesson learned from microsporidian diversity in amphipods

“…( 2020 ); (n) Quiles et al . ( 2021 ); (o) Madyarova et al . ( 2015 ); (p) Ryan and Kohler ( 2010 ); (q) Short et al .…”

“…Similarly, G. pulex clades C and E were infected with 6 and 5 microsporidian MOTUs, respectively, including 3 new associations. One new association was found even in G. roeselii clade 2 (group C in literature), which previously underwent a massive parasitological investigation (Grabner et al ., 2015 ; Bojko et al ., 2017 ; Grabner, 2017 ; Bacela-Spychalska et al ., 2018 ; Quiles et al ., 2019 , 2021 ). The present finding highlights the importance of further parasitological studies in amphipods.…”

“…Sequences of the amphipod Crangonyx islandicus (GenBank accession number HM015162) and the amphipod-infecting microsporidia Dictyocoela cavimanum (GenBank accession number KY073301) were used as outgroups. The naming of undescribed Microsporidium isolates with the exception of 2 Cucumispora isolates (sp01 and sp02) followed the classification used by previous studies (Bojko et al ., 2015 , 2017 ; Grabner, 2017 ; Bacela-Spychalska et al ., 2018 ; Quiles et al ., 2019 , 2021 ).…”

“…In contrast, vertical transmission occurs when spores are passed intergenerationally via transovarial transmission and is generally less virulent (Dunn and Smith, 2001 ). Despite being ubiquitous, microsporidians have received little attention, particularly those infecting aquatic organisms with little or no commercial value but high ecological importance, such as amphipods (Quiles et al ., 2021 ). Microsporidian diversity in amphipods is high as evidenced by several studies (Grabner et al ., 2015 ; Ironside and Wilkinson, 2018 ; Bojko and Ovcharenko, 2019 ; Park et al ., 2020 ).…”

Microsporidian diversity in the aquatic isopodAsellus aquaticus

“…Microsporidia are frequently found in aquatic systems where the majority of known species infects aquatic invertebrates (Stentiford et al, 2013;Stentiford and Dunn, 2014). While there are numerous studies on microsporidians in aquatic crustaceans such as amphipods (Krebes et al, 2010;Grabner et al, 2015Grabner et al, , 2020Madyarova et al, 2015;Weigand et al, 2016;Bacela-Spychalska et al, 2018;Quiles et al, 2019Quiles et al, , 2020Quiles et al, , 2021, to our knowledge the only microsporidium reported from Asellus aquaticus is Mrazekia argoisi that was detected in fat body cells of the host (Kudo, 1924).…”