Comparative genomics of Ascetosporea gives new insight into the evolutionary basis for animal parasitism in Rhizaria

Markus Hiltunen Thoren; Ioana Brännström; Anders Alfjorden; Hana Peckova; Fiona Swords; Chantelle Hooper; Astrid Holzer; David Bass; Fabien Burki

doi:10.1186/s12915-024-01898-x

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Title (eng)

Comparative genomics of Ascetosporea gives new insight into the evolutionary basis for animal parasitism in Rhizaria

Author

Markus Hiltunen Thoren

Ioana Brännström

Anders Alfjorden

Hana Peckova

Fiona Swords

Chantelle Hooper

Astrid Holzer

University of Veterinary Medicine Vienna

David Bass

Fabien Burki

Abstract (eng)

Ascetosporea (Endomyxa, Rhizaria) is a group of unicellular parasites infecting aquatic invertebrates. They are increasingly being recognized as widespread and important in marine environments, causing large annual losses in invertebrate aquaculture. Despite their importance, little molecular data of Ascetosporea exist, with only two genome assemblies published to date. Accordingly, the evolutionary origin of these parasites is unclear, including their phylogenetic position and the genomic adaptations that accompanied the transition from a free-living lifestyle to parasitism. Here, we sequenced and assembled three new ascetosporean genomes, as well as the genome of a closely related amphizoic species, to investigate the phylogeny, origin, and genomic adaptations to parasitism in Ascetosporea.Using a phylogenomic approach, we confirm the monophyly of Ascetosporea and show that Paramyxida group with Mikrocytida, with Haplosporida being sister to both groups. We report that the genomes of these parasites are relatively small (12-36 Mb) and gene-sparse (~ 2300-5200 genes), while containing surprisingly high amounts of non-coding sequence (~ 70-90% of the genomes). Performing gene-tree aware ancestral reconstruction of gene families, we demonstrate extensive gene losses at the origin of parasitism in Ascetosporea, primarily of metabolic functions, and little gene gain except on terminal branches. Finally, we highlight some functional gene classes that have undergone expansions during evolution of the group.We present important new genomic information from a lineage of enigmatic but important parasites of invertebrates and illuminate some of the genomic innovations accompanying the evolutionary transition to parasitism in this lineage. Our results and data provide a genetic basis for the development of control measures against these parasites.

Keywords (eng)

Genome ReductionReductive EvolutionEvolutionary TransitionPhylogenyProtozoaIntracellular ParasiteBonamiaMarteiliaParamarteiliaMikrocytosParamikrocytos

Type (eng)

journal article

Language

[eng]

Persistent identifier

https://phaidra.vetmeduni.ac.at/o:4409

DOI

10.1186/s12915-024-01898-x

Is in series

Title (eng)

BMC Biology

Volume