Although aerobic respiration is a hallmark of eukaryotes, a few unicellular lineages, growing in hypoxic environments, have secondarily lost this ability. In the absence of oxygen, the mitochondria of these organisms have lost all or parts of their genomes and evolved into mitochondria-related organelles (MROs). There has been debate regarding the presence of MROs in animals. Using deep sequencing approaches, we discovered that a member of the Cnidaria, the myxozoan Henneguya salminicola, has no mitochondrial genome, and thus has lost the ability to perform aerobic cellular respiration. This indicates that these core eukaryotic features are not ubiquitous among animals. Our analyses suggest that H. salminicola lost not only its mitochondrial genome but also nearly all nuclear genes involved in transcription and replication of the mitochondrial genome. In contrast, we identified many genes that encode proteins involved in other mitochondrial pathways and determined that genes involved in aerobic respiration or mitochondrial DNA replication were either absent or present only as pseudogenes. As a control, we used the same sequencing and annotation methods to show that a closely related myxozoan, Myxobolus squamalis, has a mitochondrial genome. The molecular results are supported by fluorescence micrographs, which show the presence of mitochondrial DNA in M. squamalis, but not in H. salminicola. Our discovery confirms that adaptation to an anaerobic environment is not unique to single-celled eukaryotes, but has also evolved in a multicellular, parasitic animal. Hence, H. salminicola provides an opportunity for understanding the evolutionary transition from an aerobic to an exclusive anaerobic metabolism.

While investigating the parasite fauna of wild coho salmon. Oncorhynchus kisutch (Walbaum, 1792), histological examination provided evidence of a new species of Myxobolus (Myxozoa: Myxosporea) infecting nerves of skeletal muscle. Spores were morphologically similar to those of the intramuscular Myxobolus insidiosus Wyatt and Pratt, 1963, both having pyriform spores with clavate polar capsules. However, the former developed exclusively in the nerves of skeletal muscle rather than in myocytes. We examined both species of Myxobolus derived from coho salmon; Chinook salmon, Oncorhynchus tshawytscha (Walbaum, 1792); cutthroat trout, Oncorhynchus clarkii (Richardson, 1836); and rainbow trout Oncorhynchus mykiss (Walbaum, 1792) from freshwater in Oregon. Spore morphology, small subunit ribosomal RNA gene (rDNA) sequences, and site of infection were compared. Myxobolus arcticus Pugachev and Khokhlov, 1979 has pyriform spores, infects the central nervous system of many salmonids, and is found in the Pacific Northwest. It was therefore included in the analyses to rule out conspecificity with the new species. Together, these data show that the Myxobolus sp. from peripheral nerves in the skeletal musculature of coho salmon, rainbow trout, and cutthroat trout is a new species, described herein as Myxobolus fryeri n. sp.

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A coelomic myxozoan infection was detected in freshwater polychaetes, Manayunkia speciosa from the Klamath River, Oregon/California, a site enzootic for the myxozoan parasites Ceratomyxa shasta and Parvicapsula minibicornis. The tetractinomyxon type actinospores had a near-spherical spore body 7.9 x 7.1 microm, with 3 spherical, protruding polar capsules, no valve cell processes, and a binucleate sporoplasm. Parvicapsula minibicornis-specific primers Parvi1f and Parvi2r amplified DNA from infected polychaetes in a polymerase chain reaction (PCR) assay. The small subunit 18S rRNA gene of the spores was sequenced (GenBank DQ231038) and was a 99.7% match with the sequence for P. minibicornis myxospore stage in GenBank (AF201375). Chinook salmon (Oncorhynchus tshawytscha) exposed to a dose of 1,000 actinospores per fish tested PCR positive for P. minibicornis at 14 wk postinfection and presporogonic stages were detected in the kidney tubules by histology at 20 wk. This life cycle is 1 of only about 30 known from more than 1,350 myxozoan species, and only the second known from a freshwater polychaete.