Peptidoglycan Production by an Insect-Bacterial Mosaic
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.
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.Attached Files
Published - 1-s2.0-S0092867419310050-main.pdf
Supplemental Material - 1-s2.0-S0092867419310050-mmc1.pdf
Supplemental Material - 1-s2.0-S0092867419310050-mmc2.xlsx
Supplemental Material - 1-s2.0-S0092867419310050-mmc3.xlsx
Files
Additional details
- PMCID
- PMC6838666
- Eprint ID
- 99050
- Resolver ID
- CaltechAUTHORS:20191003-113812895
- GBMF5602
- Gordon and Betty Moore Foundation
- NNA15BB04A
- NASA
- IOS-1553529
- NSF
- BB/N000951/1
- Biotechnology and Biological Sciences Research Council (BBSRC)
- 2058718
- Biotechnology and Biological Sciences Research Council (BBSRC)
- Created
-
2019-10-03Created from EPrint's datestamp field
- Updated
-
2022-02-16Created from EPrint's last_modified field
- Caltech groups
- Kavli Nanoscience Institute, Division of Geological and Planetary Sciences