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Molecular evolutionary trends and biosynthesis pathways in the Oribatida revealed by the genome of Archegozetes longisetosus

Brückner, Adrian and Barnett, Austen A. and Antoshechkin, Igor A. and Kitchen, Sheila A. (2020) Molecular evolutionary trends and biosynthesis pathways in the Oribatida revealed by the genome of Archegozetes longisetosus. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20201214-074948609

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Abstract

Background: Oribatid mites are a specious order of microarthropods within the subphylum Chelicerata, compromising about 11,000 described species. They are ubiquitously distributed across different microhabitats in all terrestrial ecosystems around the world and were among the first animals colonizing terrestrial habitats as decomposers and scavengers. Noted for their biosynthesis capacities and biochemical diversity, the majority of oribatid mites possess a pair of exocrine opisthonotal oil-glands used for chemical defense and communication. Genomic resources are lacking for oribatids despite their species richness and ecological importance. Results: We used a comparative genomic approach to investigate the developmental, sensory and glandular biosynthetic gene repertoire of the clonal, all-female oribatid mite species Archegozetes longisetosus Aoki, a model species used by numerous laboratories for the past 30 years. Here, we present a 190-Mb genome assembly constructed from Nanopore MinION and Illumina sequencing platforms with 23,825 predicted protein-coding genes. Genomic and transcriptional analyses revealed patterns of reduced body segmentation and loss of segmental identity gene abd-A within Acariformes, and unexpected expression of key eye development genes in these eyeless mites across developmental stages. Consistent with the soil dwelling lifestyle, investigation of the sensory genes revealed a species-specific expansion of gustatory receptors, the largest chemoreceptor family in the genome used in olfaction, and evidence of horizontally transferred enzymes used in cell wall degradation of plant and fungal matter, both components of the Archegozetes longisetosus diet. Using biochemical and genomic data, we were able to delineate the backbone biosynthesis of monoterpenes, an important class of compounds found in the major exocrine gland system of Oribatida - the oil glands. Conclusions: With the Archegozetes longisetosus genome, we now have the first high-quality, annotated genome of an oribatid mite genome. Given the mite's strength as an experimental model, the new sequence resources provided here will serve as the foundation for molecular research in Oribatida and will enable a broader understanding of chelicerate evolution.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2020.12.10.420141DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/bioproject/PRJNA683999Related ItemData/Code
https://www.ncbi.nlm.nih.gov/bioproject/PRJNA683935Related ItemData/Code
https://doi.org/10.22002/D1.1876Related ItemData
ORCID:
AuthorORCID
Brückner, Adrian0000-0002-9184-8562
Barnett, Austen A.0000-0003-4290-7594
Antoshechkin, Igor A.0000-0002-9934-3040
Kitchen, Sheila A.0000-0003-4402-8139
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Version 1: December 11, 2020. Version 2: February 9, 2021. We thank Joe Parker for making his laboratory space and resources available to us. Michael Heethoff, Sebastian Schemlzle, Benjamin Weiss and Martin Kaltenpoth graciously allowed us to use some of their unpublished images. Roy A. Norton provided invaluable comments to the manuscript and collected the first specimens of Archegozetes longisetosus giving rise to the current laboratory strain. This work was supported by a grant from the Caltech Center for Environmental Microbial Interactions (CEMI) to AB. AB is Simons Fellow of the Life Sciences Research Foundation (LSRF). Authors contributions: AB had the initial idea for the study; AB, AAB and SAK design research; IAA performed long-read sequencing and assembled the genome; AB performed all other experimental work; AAB analyzed hox and life-stage specific expression data; AB analyzed chemical data; SAK and AB performed bioinformatic analyses; AB wrote the first draft of the manuscript with input from AAB and SAK; SAK revised the manuscript. All authors gave final approval for publication. Ethics statement: There are no legal restrictions on working with mites. Data availability: Genomic and transcriptomic data generated for his project can be found on NCBI under the accession numbers PRJNA683935 and PRJNA683999. All other data related to this manuscript can be found at https://doi.org/10.22002/D1.1876 under a cc-by-nc-4.0 license (Brückner 2021).
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funders:
Funding AgencyGrant Number
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Simons FoundationUNSPECIFIED
Life Sciences Research FoundationUNSPECIFIED
Subject Keywords:soil animal, terpene synthesis, horizontal gene transfer, parthenogenesis, chemoreceptors, Hox genes, model organism, RNAseq, MinION long-read sequencing, Sarcoptiformes
Record Number:CaltechAUTHORS:20201214-074948609
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201214-074948609
Official Citation:Molecular evolutionary trends and biosynthesis pathways in the Oribatida revealed by the genome of Archegozetes longisetosus. Adrian Brückner, Austen A. Barnett, Igor A. Antoshechkin, Sheila A. Kitchen. bioRxiv 2020.12.10.420141; doi: https://doi.org/10.1101/2020.12.10.420141
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:107054
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:14 Dec 2020 21:11
Last Modified:10 Feb 2021 18:34

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