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Peptidoglycan Production by an Insect-Bacterial Mosaic

Bublitz, DeAnna C. and Chadwick, Grayson L. and Magyar, John S. and Sandoz, Kelsi M. and Brooks, Diane M. and Mesnage, Stéphane and Ladinsky, Mark S. and Garber, Arkadiy I. and Bjorkman, Pamela J. and Orphan, Victoria J. and McCutcheon, John P. (2019) Peptidoglycan Production by an Insect-Bacterial Mosaic. Cell, 179 (3). pp. 703-712. ISSN 0092-8674. PMCID PMC6838666. https://resolver.caltech.edu/CaltechAUTHORS:20191003-113812895

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Abstract

Peptidoglycan (PG) is a defining feature of bacteria, involved in cell division, shape, and integrity. We previously reported that several genes related to PG biosynthesis were horizontally transferred from bacteria to the nuclear genome of mealybugs. Mealybugs are notable for containing a nested bacteria-within-bacterium endosymbiotic structure in specialized insect cells, where one bacterium, Moranella, lives in the cytoplasm of another bacterium, Tremblaya. Here we show that horizontally transferred genes on the mealybug genome work together with genes retained on the Moranella genome to produce a PG layer exclusively at the Moranella cell periphery. Furthermore, we show that an insect protein encoded by a horizontally transferred gene of bacterial origin is transported into the Moranella cytoplasm. These results provide a striking parallel to the genetic and biochemical mosaicism found in organelles, and prove that multiple horizontally transferred genes can become integrated into a functional pathway distributed between animal and bacterial endosymbiont genomes.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cell.2019.08.054DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6838666PubMed CentralArticle
ORCID:
AuthorORCID
Bublitz, DeAnna C.0000-0003-3419-2103
Chadwick, Grayson L.0000-0003-0700-9350
Magyar, John S.0000-0002-3586-8286
Sandoz, Kelsi M.0000-0002-6960-0560
Mesnage, Stéphane0000-0003-1648-4890
Ladinsky, Mark S.0000-0002-1036-3513
Garber, Arkadiy I.0000-0001-7935-0246
Bjorkman, Pamela J.0000-0002-2277-3990
Orphan, Victoria J.0000-0002-5374-6178
McCutcheon, John P.0000-0002-5489-6039
Additional Information:© 2019 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Received 18 June 2019, Revised 6 August 2019, Accepted 28 August 2019, Available online 3 October 2019. Data and Code Availability: 16S rRNA amplicon sequences have been deposited in NCBI under BioProject ID: PRJNA546070. All membrane measurements presented in Figure 4 are included in this manuscript as Table S3. We thank Bil Clemons for helpful discussions about PG; Denghui David Xing of the University of Montana Genomics Core for sequencing expertise; Carol Garland, Matthew Hunt, and the Caltech Kavli Nanoscience Institute for aid in maintaining the TF-30 electron microscope; and the Gordon and Betty Moore and Beckman Foundations for gifts to Caltech to support electron microscopy. PG Mass spectrometry analyses were performed by the biOMICS Facility of the Faculty of Science Mass Spectrometry Centre at the University of Sheffield. We thank Adelina E. Acosta-Martin and Ankur Patel for their help with peptidoglycan analyses. This work was supported by the Gordon and Betty Moore Foundation (GBMF5602), the National Aeronautics and Space Administration Astrobiology Institute (NNA15BB04A), the National Science Foundation (IOS-1553529), and the Biotechnology and Biological Sciences Research Council (BB/N000951/1 and 2058718). Author Contributions: D.C.B.: conceptualization, investigation, analysis, methodology, validation, visualization, and writing; G.L.C. and J.S.M.: investigation, methodology, analysis, validation, visualization, and writing; K.M.S.: conceptualization, analysis, methodology, investigation, resources, and writing; S.M.: analysis, methodology, resources, software, and writing; D.M.B.: investigation, methodology, and visualization; M.S.L.: investigation, methodology, resources, validation, and visualization; A.I.G.: data curation, analysis, investigation, software, and visualization; P.J.B.: methodology, resources, and administration; V.J.O.: conceptualization, funding acquisition, resources, and administration; J.P.M.: conceptualization, funding acquisition, administration, resources, visualization, and writing. The authors declare no competing interests.
Group:Kavli Nanoscience Institute
Funders:
Funding AgencyGrant Number
Gordon and Betty Moore FoundationGBMF5602
NASANNA15BB04A
NSFIOS-1553529
Biotechnology and Biological Sciences Research Council (BBSRC)BB/N000951/1
Biotechnology and Biological Sciences Research Council (BBSRC)2058718
Issue or Number:3
PubMed Central ID:PMC6838666
Record Number:CaltechAUTHORS:20191003-113812895
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191003-113812895
Official Citation:DeAnna C. Bublitz, Grayson L. Chadwick, John S. Magyar, Kelsi M. Sandoz, Diane M. Brooks, Stéphane Mesnage, Mark S. Ladinsky, Arkadiy I. Garber, Pamela J. Bjorkman, Victoria J. Orphan, John P. McCutcheon, Peptidoglycan Production by an Insect-Bacterial Mosaic, Cell, Volume 179, Issue 3, 2019, Pages 703-712.e7, ISSN 0092-8674, https://doi.org/10.1016/j.cell.2019.08.054. (http://www.sciencedirect.com/science/article/pii/S0092867419310050)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:99050
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:03 Oct 2019 19:45
Last Modified:05 Dec 2019 21:32

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