Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements

Abstract In the spore-forming bacterium Bacillus subtilis transcription and translation are uncoupled and the translational machinery is located at the cell poles. During sporulation, the cell undergoes morphological changes including asymmetric division and chromosome translocation into the forespo...

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Main Authors: Olga Iwańska, Przemysław Latoch, Mariia Kovalenko, Małgorzata Lichocka, Joanna Hołówka, Remigiusz Serwa, Agata Grzybowska, Jolanta Zakrzewska-Czerwińska, Agata L. Starosta
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55196-9
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author Olga Iwańska
Przemysław Latoch
Mariia Kovalenko
Małgorzata Lichocka
Joanna Hołówka
Remigiusz Serwa
Agata Grzybowska
Jolanta Zakrzewska-Czerwińska
Agata L. Starosta
author_facet Olga Iwańska
Przemysław Latoch
Mariia Kovalenko
Małgorzata Lichocka
Joanna Hołówka
Remigiusz Serwa
Agata Grzybowska
Jolanta Zakrzewska-Czerwińska
Agata L. Starosta
author_sort Olga Iwańska
collection DOAJ
description Abstract In the spore-forming bacterium Bacillus subtilis transcription and translation are uncoupled and the translational machinery is located at the cell poles. During sporulation, the cell undergoes morphological changes including asymmetric division and chromosome translocation into the forespore. However, the fate of translational machinery during sporulation has not been described. Here, using microscopy and mass spectrometry, we show the localisation of ribosomes during sporulation in wild type and mutant Bacillus subtilis. We demonstrate that ribosomes are associated with the asymmetric septum, a functionally important organelle in the cell’s developmental control, and that SpoIIDMP-driven peptidoglycan rearrangement is crucial for ribosomes packing into the forespore. We also show that the SpoIIIA-SpoIIQ ‘feeding-tube’ channel is not required for ribosome translocation. Our results demonstrate that translation and translational machinery are temporally and spatially organised in B. subtilis during sporulation and that the forespore ‘inherits’ ribosomes from the mother cell. We propose that the movement of ribosomes in the cell may be mediated by the bacterial homologs of cytoskeletal proteins and that the cues for asymmetric division localisation may be translation-dependent. We anticipate our findings to elicit more sophisticated structural and mechanistic studies of ribosome organisation during bacterial cell development.
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spelling doaj-art-3dba8c1f474d42caa442306a5b4dcb172025-01-05T12:38:30ZengNature PortfolioNature Communications2041-17232025-01-0116111110.1038/s41467-024-55196-9Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangementsOlga Iwańska0Przemysław Latoch1Mariia Kovalenko2Małgorzata Lichocka3Joanna Hołówka4Remigiusz Serwa5Agata Grzybowska6Jolanta Zakrzewska-Czerwińska7Agata L. Starosta8Institute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesDepartment of Molecular Microbiology, Faculty of Biotechnology, University of WroclawInternational Institute of Molecular Mechanisms and Machines, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesDepartment of Molecular Microbiology, Faculty of Biotechnology, University of WroclawInstitute of Biochemistry and Biophysics, Polish Academy of SciencesAbstract In the spore-forming bacterium Bacillus subtilis transcription and translation are uncoupled and the translational machinery is located at the cell poles. During sporulation, the cell undergoes morphological changes including asymmetric division and chromosome translocation into the forespore. However, the fate of translational machinery during sporulation has not been described. Here, using microscopy and mass spectrometry, we show the localisation of ribosomes during sporulation in wild type and mutant Bacillus subtilis. We demonstrate that ribosomes are associated with the asymmetric septum, a functionally important organelle in the cell’s developmental control, and that SpoIIDMP-driven peptidoglycan rearrangement is crucial for ribosomes packing into the forespore. We also show that the SpoIIIA-SpoIIQ ‘feeding-tube’ channel is not required for ribosome translocation. Our results demonstrate that translation and translational machinery are temporally and spatially organised in B. subtilis during sporulation and that the forespore ‘inherits’ ribosomes from the mother cell. We propose that the movement of ribosomes in the cell may be mediated by the bacterial homologs of cytoskeletal proteins and that the cues for asymmetric division localisation may be translation-dependent. We anticipate our findings to elicit more sophisticated structural and mechanistic studies of ribosome organisation during bacterial cell development.https://doi.org/10.1038/s41467-024-55196-9
spellingShingle Olga Iwańska
Przemysław Latoch
Mariia Kovalenko
Małgorzata Lichocka
Joanna Hołówka
Remigiusz Serwa
Agata Grzybowska
Jolanta Zakrzewska-Czerwińska
Agata L. Starosta
Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements
Nature Communications
title Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements
title_full Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements
title_fullStr Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements
title_full_unstemmed Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements
title_short Ribosomes translocation into the spore of Bacillus subtilis is highly organised and requires peptidoglycan rearrangements
title_sort ribosomes translocation into the spore of bacillus subtilis is highly organised and requires peptidoglycan rearrangements
url https://doi.org/10.1038/s41467-024-55196-9
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