A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome

Dayana Yahalomi; Stephen D. Atkinson; Moran Neuhof; E. Sally Chang; Hervé Philippe; Paulyn Cartwright; Jerri L. Bartholomew; Dorothée Huchon

doi:10.1073/pnas.1909907117

Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved January 10, 2020 (received for review June 25, 2019)

Significance

Mitochondrial respiration is an ancient characteristic of eukaryotes. However, it was lost independently in multiple eukaryotic lineages as part of adaptations to an anaerobic lifestyle. We show that a similar adaptation occurred in a member of the Myxozoa, a large group of microscopic parasitic animals that are closely related to jellyfish and hydroids. Using deep sequencing approaches supported by microscopic observations, we present evidence that an animal has lost its mitochondrial genome. The myxozoan cells retain structures deemed mitochondrion-related organelles, but have lost genes related to aerobic respiration and mitochondrial genome replication. Our discovery shows that aerobic respiration, one of the most important metabolic pathways, is not ubiquitous among animals.

Abstract

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.

Footnotes

↵¹D.Y. and S.D.A. contributed equally to this work.
↵²To whom correspondence may be addressed. Email: huchond{at}tauex.tau.ac.il.

Author contributions: P.C., J.L.B., and D.H. designed research; D.Y., S.D.A., and D.H. performed research; D.Y., J.L.B., and D.H. contributed new reagents/analytic tools; D.Y., M.N., E.S.C., H.P., and D.H. analyzed data; and D.Y., S.D.A., and D.H. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
Data deposition: Voucher paratype material was deposited at the US National Parasite Collection, Smithsonian Institution, Washington, DC (https://collections.nmnh.si.edu/search/iz/) under the following accession numbers: Henneguya salminicola myxospores: USNM1611578 (from genome sample) and USNM1611579 (from transcriptome sample); Myxobolus squamalis myxospores: USNM1611580 (from genome sample); M. squamalis myxospores and developmental stages: USNM1611581 (from transcriptome sample). All sequence data have been deposited in the National Center for Biotechnology Information (NCBI) database (https://www.ncbi.nlm.nih.gov/). The H. salminicola data are available under the BioProject accession number PRJNA485580. The SSU rDNA sequence was deposited under MK480607. The raw transcriptome and genome reads are available under accession numbers SRR7754566 and SRR7754567, respectively. The transcriptome and genome shotgun assembly projects were deposited at under the accession GHBP00000000 and SGJC00000000, respectively. The M. squamalis data are available under the BioProject accession number PRJNA485581. The SSU rDNA sequence was deposited under MK480606. The raw transcriptome and genome reads are available under the accession numbers SRR7760054 and SRR7760053, respectively. The transcriptome and genome shotgun assembly projects were deposited under accession numbers GHBR00000000 and QWKW00000000, respectively. The mt genome of M. squamalis was deposited under the accession number MK087050. These accession numbers are provided in Dataset S6. The Bayesian trees and all alignments were deposited in the Dryad Digital Repository (https://doi.org/10.5061/dryad.v15dv41sm). Finally, the uncropped images underlying Fig. 2 and SI Appendix, Figs. S7 and S8 were deposited in the Figshare repository (https://doi.org/10.6084/m9.figshare.8300003, https://doi.org/10.6084/m9.figshare.9897284, https://doi.org/10.6084/m9.figshare.9897320).
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