Wolbachia and Cardinium infection found in threatened unionid species: a new concern for conservation of freshwater mussels?

Abstract

Endosymbiotic bacterial species that manipulate host biology, reproduction and mitochondrial genetic diversity have been identified in many metazoans, especially terrestrial arthropods. Until now, the hypothesis that Wolbachia or other bacterial endosymbiont might be absent in mollusks has remained unexplored. We present here preliminary data on bacterial communities in a freshwater mussel Unio crassus-species with doubly uniparental inheritance of mtDNA (DUI). Next generation sequencing of 16S rRNA bacterial gene fragment allowed to identify endosymbiotic Cardinium and sequences that were classified to the order Rickettsiales. Finally, we discovered Wolbachia and confirmed Cardinium infection of Unio crassus using bacterial species-specific primers. Discovering Wolbachia and Cardinium infections in Unio crassus opens new opportunities of further investigations in the second largest animal phylum on Earth, very diversified phylogenetically, widespread geographically and inhabiting many environs, including freshwater, inhabited by the most threatened molluscan species. Considering the problems caused by endosymbionts identified in arthropods, the presence of endosymbiotic factor implies possibility of their influence on taxonomy of threatened unionids, on the results of studies of genetic diversity and proper conservation planning.

Multisystemic inflammatory disease in Pheasantshell (Unionidae,Actinonaias pectorosa) associated withYokenella regensburgeiinfection at sites experiencing seasonal mass mortality events

“…This OTU was especially abundant in controls representing nearly half (45%) of all recovered sequences in those digestive glands, and was the only OTU significantly associated with this group via indicator species analysis. Rickettsia-like organisms have been sporadically reported via histological examination of the digestive gland of mussels previously (Mioduchowska et al 2020;Burcham et al 2023) and could represent an important commensal in healthy tissue. This rickettsial OTU was also found with high relative abundance in the hemolymph of controls while lower in hemolymph of both case groups (Case-Present, Case-Absent) and warrants further investigation for use as a potential indicator of mussel health.…”

Playing Peekaboo with a Master Manipulator: Metagenetic Detection and Phylogenetic Analysis of Wolbachia Supergroups in Freshwater Invertebrates

“…In 1995, Sironi et al [33] found a Wolbachia-like organism in Nematoda for the very first time. In 2018-2021, our team discovered Wolbachia infections in Tardigrada [34], Bivalvia [35] and Crustacea [32]. Later, Tibbs-Cortes et al [36] also confirmed Wolbachia infection in the microbiome of Tardigrada.…”

“…The only Wolbachia sequences in bivalves were those reported by Mioduchowska et al [35] for U. crassus. These sequences have been clustered in a clade containing a possible new strain, which is here named supergroup V. In this study, Wolbachia was rediscovered in U. crassus (previously reported in [35]) and was discovered for the first time in D. polymorpha. Both infections were detected using our designed primers.…”

Freshwater mussel conservation: A global horizon scan of emerging threats and opportunities

“…However, no standard set of biomarkers or other diagnostic tools exist to assess mussel health in response to a wide range of known and unknown stressors. Because mussels are filter feeders, their symbiotic microbiome also may be sensitive to environmental conditions and could provide additional insight about overall health status (Aceves, 2019 ; McCauley et al, 2021 ; Mioduchowska et al, 2020 ; Weingarten et al, 2019 ). A standardized diagnostic approach specific to mussels is needed that can identify clinical signs of compromised health.…”

“…Pathogens, including trematodes, nematodes, mites, ciliates, bacteria, and viruses can have a wide range of negative effects on mussels (and other species), including catastrophic mortality (Brian & Aldridge, 2019 ; Richard et al, 2020 ; Taskinen et al, 1997 ). In addition, bacterial endosymbionts, that is, Wolbachia and Cardinium , recently recorded in the threatened Unio crassus (Mioduchowska et al, 2020 ), can significantly increase parthenogenesis and female‐biased sex ratios through feminization, male killing, and cytoplasmic incompatibility. The infection and severity of these endosymbionts are expected to be affected by climate change (Charlesworth et al, 2019 ).…”