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The evolution of interdependence in a four-way mealybug symbiosis

Garber, Arkadiy I. and Kupper, Maria and Laetsch, Dominik R. and Weldon, Stephanie R. and Ladinsky, Mark S. and Bjorkman, Pamela J. and McCutcheon, John P. (2021) The evolution of interdependence in a four-way mealybug symbiosis. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210201-122621328

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Abstract

Mealybugs are insects that maintain intracellular bacterial symbionts to supplement their nutrientpoor plant sap diets. Some mealybugs have a single betaproteobacterial endosymbiont, a Candidatus Tremblaya species (hereafter Tremblaya) that alone provides the insect with its required nutrients. Other mealybugs have two nutritional endosymbionts that together provide these nutrients, where Tremblaya has gained a gammaproteobacterial partner that resides in the cytoplasm of Tremblaya. Previous work had established that Pseudococcus longispinus mealybugs maintain not one but two species of gammaproteobacterial endosymbionts along with Tremblaya. Preliminary genomic analyses suggested that these two gammaproteobacterial endosymbionts have large genomes with features consistent with a relatively recent origin as insect endosymbionts, but the patterns of genomic complementarity between members of the symbiosis and their relative cellular locations were unknown. Here, using long-read sequencing and various types of microscopy, we show that the two gammaproteobacterial symbionts of P. longispinus are mixed together within Tremblaya cells, and that their genomes are somewhat reduced in size compared to their closest non-endosymbiotic relatives. Both gammaproteobacterial genomes contain thousands of pseudogenes, consistent with a relatively recent shift from a free-living to endosymbiotic lifestyle. Biosynthetic pathways of key metabolites are partitioned in complex interdependent patterns among the two gammaproteobacterial genomes, the Tremblaya genome, and horizontally acquired bacterial genes that are encoded on the mealybug nuclear genome. Although these two gammaproteobacterial endosymbionts have been acquired recently in evolutionary time, they have already evolved co-dependencies with each other, Tremblaya, and their insect host.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.01.28.428658DOIDiscussion Paper
https://doi.org/10.6084/m9.figshare.13632407.v1DOIData
https://doi.org/10.6084/m9.figshare.13632398.v2DOIData
https://doi.org/10.6084/m9.figshare.13632419.v1DOIData
https://doi.org/10.6084/m9.figshare.13632416.v1DOIData
https://doi.org/10.6084/m9.figshare.13661189DOIData
https://github.com/Arkadiy-Garber/PLON-genome-paperRelated ItemCode
ORCID:
AuthorORCID
Garber, Arkadiy I.0000-0001-7935-0246
Laetsch, Dominik R.0000-0001-7887-0186
Weldon, Stephanie R.0000-0001-5384-9946
Ladinsky, Mark S.0000-0002-1036-3513
Bjorkman, Pamela J.0000-0002-2277-3990
McCutcheon, John P.0000-0002-5489-6039
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 4.0 International license. This version posted January 29, 2021. We thank Diane Brooks, Paul Caccamo, Filip Husník, Genevieve Krause, Piotr Łukasik, Mitch Syberg-Olsen, Dan Vanderpool, Catherine Armbruster, and Travis Wheeler for helpful discussions and insights during the course of this project. We thank the Caltech Kavli Nanoscience Institute for maintenance of the TF-30 electron microscope. This work was supported by the National Science Foundation (IOS-1553529; to JPM), the Gordon and Betty Moore Foundation (GBMF5602; to JPM), the National Aeronautics and Space Administration Astrobiology Institute (NNA15BB04A; to JPM), and the National Institute of Allergy and Infectious Diseases (2 P50 AI150464; to PJB). The authors have declared no competing interest.
Group:Kavli Nanoscience Institute
Funders:
Funding AgencyGrant Number
NSFIOS-1553529
Gordon and Betty Moore FoundationGBMF5602
NASANNA15BB04A
NIH2 P50 AI150464
Subject Keywords:endosymbionts, pseudogenes, transposases, genome reduction, metabolic interdependence, mealybugs
Record Number:CaltechAUTHORS:20210201-122621328
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210201-122621328
Official Citation:The evolution of interdependence in a four-way mealybug symbiosis. Arkadiy I. Garber, Maria Kupper, Dominik R. Laetsch, Stephanie R. Weldon, Mark S. Ladinsky, Pamela J. Bjorkman, John P. McCutcheon. bioRxiv 2021.01.28.428658; doi: https://doi.org/10.1101/2021.01.28.428658
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:107835
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Feb 2021 21:40
Last Modified:01 Feb 2021 21:40

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