Macromolecular Crowding, Phase Separation, and Homeostasis in the Orchestration of Bacterial Cellular Functions

Macromolecular crowding affects the activity of proteins and functional macromolecular complexes in all cells, including bacteria. Crowding, together with physicochemical parameters such as pH, ionic strength, and the energy status, influences the structure of the cytoplasm and thereby indirectly ma...

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Published inChemical reviews Vol. 124; no. 4; pp. 1899 - 1949
Main Authors Monterroso, Begoña, Margolin, William, Boersma, Arnold J., Rivas, Germán, Poolman, Bert, Zorrilla, Silvia
Format Journal Article
LanguageEnglish
Published United States American Chemical Society 28.02.2024
Subjects
Bacteria
Cell division
Condensates
Crowding
Environmental stress
Functionals
Homeostasis
Phase separation
Physicochemical properties
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Abstract Macromolecular crowding affects the activity of proteins and functional macromolecular complexes in all cells, including bacteria. Crowding, together with physicochemical parameters such as pH, ionic strength, and the energy status, influences the structure of the cytoplasm and thereby indirectly macromolecular function. Notably, crowding also promotes the formation of biomolecular condensates by phase separation, initially identified in eukaryotic cells but more recently discovered to play key functions in bacteria. Bacterial cells require a variety of mechanisms to maintain physicochemical homeostasis, in particular in environments with fluctuating conditions, and the formation of biomolecular condensates is emerging as one such mechanism. In this work, we connect physicochemical homeostasis and macromolecular crowding with the formation and function of biomolecular condensates in the bacterial cell and compare the supramolecular structures found in bacteria with those of eukaryotic cells. We focus on the effects of crowding and phase separation on the control of bacterial chromosome replication, segregation, and cell division, and we discuss the contribution of biomolecular condensates to bacterial cell fitness and adaptation to environmental stress.
AbstractList Macromolecular crowding affects the activity of proteins and functional macromolecular complexes in all cells, including bacteria. Crowding, together with physicochemical parameters such as pH, ionic strength, and the energy status, influences the structure of the cytoplasm and thereby indirectly macromolecular function. Notably, crowding also promotes the formation of biomolecular condensates by phase separation, initially identified in eukaryotic cells but more recently discovered to play key functions in bacteria. Bacterial cells require a variety of mechanisms to maintain physicochemical homeostasis, in particular in environments with fluctuating conditions, and the formation of biomolecular condensates is emerging as one such mechanism. In this work, we connect physicochemical homeostasis and macromolecular crowding with the formation and function of biomolecular condensates in the bacterial cell and compare the supramolecular structures found in bacteria with those of eukaryotic cells. We focus on the effects of crowding and phase separation on the control of bacterial chromosome replication, segregation, and cell division, and we discuss the contribution of biomolecular condensates to bacterial cell fitness and adaptation to environmental stress.
Macromolecular crowding affects the activity of proteins and functional macromolecular complexes in all cells, including bacteria. Crowding, together with physicochemical parameters such as pH, ionic strength, and the energy status, influences the structure of the cytoplasm and thereby indirectly macromolecular function. Notably, crowding also promotes the formation of biomolecular condensates by phase separation, initially identified in eukaryotic cells but more recently discovered to play key functions in bacteria. Bacterial cells require a variety of mechanisms to maintain physicochemical homeostasis, in particular in environments with fluctuating conditions, and the formation of biomolecular condensates is emerging as one such mechanism. In this work, we connect physicochemical homeostasis and macromolecular crowding with the formation and function of biomolecular condensates in the bacterial cell and compare the supramolecular structures found in bacteria with those of eukaryotic cells. We focus on the effects of crowding and phase separation on the control of bacterial chromosome replication, segregation, and cell division, and we discuss the contribution of biomolecular condensates to bacterial cell fitness and adaptation to environmental stress.Macromolecular crowding affects the activity of proteins and functional macromolecular complexes in all cells, including bacteria. Crowding, together with physicochemical parameters such as pH, ionic strength, and the energy status, influences the structure of the cytoplasm and thereby indirectly macromolecular function. Notably, crowding also promotes the formation of biomolecular condensates by phase separation, initially identified in eukaryotic cells but more recently discovered to play key functions in bacteria. Bacterial cells require a variety of mechanisms to maintain physicochemical homeostasis, in particular in environments with fluctuating conditions, and the formation of biomolecular condensates is emerging as one such mechanism. In this work, we connect physicochemical homeostasis and macromolecular crowding with the formation and function of biomolecular condensates in the bacterial cell and compare the supramolecular structures found in bacteria with those of eukaryotic cells. We focus on the effects of crowding and phase separation on the control of bacterial chromosome replication, segregation, and cell division, and we discuss the contribution of biomolecular condensates to bacterial cell fitness and adaptation to environmental stress.
Author Margolin, William
Zorrilla, Silvia
Monterroso, Begoña
Boersma, Arnold J.
Rivas, Germán
Poolman, Bert
AuthorAffiliation Department of Structural and Chemical Biology, Centro de Investigaciones Biológicas Margarita Salas
University of Groningen
Cellular Protein Chemistry, Bijvoet Centre for Biomolecular Research, Faculty of Science
UTHealth-Houston
Department of Microbiology and Molecular Genetics, McGovern Medical School
Department of Biochemistry
Utrecht University
AuthorAffiliation_xml – name: Cellular Protein Chemistry, Bijvoet Centre for Biomolecular Research, Faculty of Science
– name: Department of Structural and Chemical Biology, Centro de Investigaciones Biológicas Margarita Salas
– name: Department of Microbiology and Molecular Genetics, McGovern Medical School
– name: University of Groningen
– name: Department of Biochemistry
– name: UTHealth-Houston
– name: Utrecht University
Author_xml – sequence: 1
  givenname: Begoña
  orcidid: 0000-0003-2538-084X
  surname: Monterroso
  fullname: Monterroso, Begoña
  email: bmonterroso@iqf.csic.es
  organization: Department of Structural and Chemical Biology, Centro de Investigaciones Biológicas Margarita Salas
– sequence: 2
  givenname: William
  orcidid: 0000-0001-6557-7706
  surname: Margolin
  fullname: Margolin, William
  organization: UTHealth-Houston
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  givenname: Arnold J.
  orcidid: 0000-0002-3714-5938
  surname: Boersma
  fullname: Boersma, Arnold J.
  organization: Utrecht University
– sequence: 4
  givenname: Germán
  orcidid: 0000-0003-3450-7478
  surname: Rivas
  fullname: Rivas, Germán
  organization: Department of Structural and Chemical Biology, Centro de Investigaciones Biológicas Margarita Salas
– sequence: 5
  givenname: Bert
  orcidid: 0000-0002-1455-531X
  surname: Poolman
  fullname: Poolman, Bert
  email: b.poolman@rug.nl
  organization: University of Groningen
– sequence: 6
  givenname: Silvia
  orcidid: 0000-0002-6309-9058
  surname: Zorrilla
  fullname: Zorrilla, Silvia
  email: silvia@cib.csic.es
  organization: Department of Structural and Chemical Biology, Centro de Investigaciones Biológicas Margarita Salas
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38331392$$D View this record in MEDLINE/PubMed
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Snippet Macromolecular crowding affects the activity of proteins and functional macromolecular complexes in all cells, including bacteria. Crowding, together with...
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SubjectTerms Bacteria
Cell division
Condensates
Crowding
Environmental stress
Functionals
Homeostasis
Phase separation
Physicochemical properties
Title Macromolecular Crowding, Phase Separation, and Homeostasis in the Orchestration of Bacterial Cellular Functions
URI http://dx.doi.org/10.1021/acs.chemrev.3c00622
https://www.ncbi.nlm.nih.gov/pubmed/38331392
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