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Genomic insights into cyanobacterial protein translocation systems

Genomic insights into cyanobacterial protein translocation systems AbstractCyanobacteria are ubiquitous oxygenic photosynthetic bacteria with a versatile metabolism that is highly dependent on effective protein targeting. Protein sorting in diderm bacteria is not trivial and, in cyanobacteria, even less so due to the presence of a complex membrane system: the outer membrane, the plasma membrane and the thylakoid membrane. In cyanobacteria, protein import into the thylakoids is essential for photosynthesis, export to the periplasm fulfills a multifunctional role in maintaining cell homeostasis, and secretion mediates motility, DNA uptake and environmental interactions. Intriguingly, only one set of genes for the general secretory and the twin-arginine translocation pathways seem to be present. However, these systems have to operate in both plasma and thylakoid membranes. This raises the question of how substrates are recognized and targeted to their correct, final destination. Additional complexities arise when a protein has to be secreted across the outer membrane, where very little is known regarding the mechanisms involved. Given their ecological importance and biotechnological interest, a better understanding of protein targeting in cyanobacteria is of great value. This review will provide insights into the known knowns of protein targeting, propose hypotheses based on available genomic sequences and discuss future directions. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Biological Chemistry de Gruyter

Genomic insights into cyanobacterial protein translocation systems

Russo, David A.; Zedler, Julie A. Z.
Biological Chemistry , Volume 402 (1): 16 – Nov 18, 2020
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Publisher
de Gruyter
Copyright
© 2020 Walter de Gruyter GmbH, Berlin/Boston
ISSN
1431-6730
eISSN
1437-4315
DOI
10.1515/hsz-2020-0247
Publisher site
See Article on Publisher Site

Abstract

AbstractCyanobacteria are ubiquitous oxygenic photosynthetic bacteria with a versatile metabolism that is highly dependent on effective protein targeting. Protein sorting in diderm bacteria is not trivial and, in cyanobacteria, even less so due to the presence of a complex membrane system: the outer membrane, the plasma membrane and the thylakoid membrane. In cyanobacteria, protein import into the thylakoids is essential for photosynthesis, export to the periplasm fulfills a multifunctional role in maintaining cell homeostasis, and secretion mediates motility, DNA uptake and environmental interactions. Intriguingly, only one set of genes for the general secretory and the twin-arginine translocation pathways seem to be present. However, these systems have to operate in both plasma and thylakoid membranes. This raises the question of how substrates are recognized and targeted to their correct, final destination. Additional complexities arise when a protein has to be secreted across the outer membrane, where very little is known regarding the mechanisms involved. Given their ecological importance and biotechnological interest, a better understanding of protein targeting in cyanobacteria is of great value. This review will provide insights into the known knowns of protein targeting, propose hypotheses based on available genomic sequences and discuss future directions.

Journal

Biological Chemistry – de Gruyter

Published: Nov 18, 2020

References

  • IM30 triggers membrane fusion in cyanobacteria and chloroplasts
  • Factors controlling floc formation and structure in the cyanobacterium Synechocystis sp. PCC 6803
  • HesF, an exoprotein required for filament adhesion and aggregation in Anabaena sp. PCC 7120
  • GDSL family of serine esterases/lipases
  • Membrane-specific targeting of green fluorescent protein by the Tat pathway in the cyanobacterium Synechocystis PCC6803
  • Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803
  • Developing Gram-negative bacteria for the secretion of heterologous proteins
  • Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins
  • Genomic structure of an economically important cyanobacterium, Arthrospira (Spirulina) platensis NIES-39
  • Transport of folded proteins by the Tat system
  • Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey
  • From bacteria to chloroplasts: evolution of the chloroplast SRP system
  • Signal peptides for recombinant protein secretion in bacterial expression systems
  • Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli
  • Protein translocation and thylakoid biogenesis in cyanobacteria
  • Functional role of PilA in iron acquisition in the cyanobacterium Synechocystis sp. PCC 6803
  • mRNA localisation, reaction centre biogenesis and thylakoid membrane targeting in cyanobacteria
  • Protein secretion through autotransporter and two-partner pathways
  • Inactivation of a predicted leader peptidase prevents photoautotrophic growth of Synechocystis sp. strain PCC 6803
  • Architecture, function, and substrates of the type II secretion system
  • The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120
  • Extracellular proteins: novel key components of metal resistance in cyanobacteria?
  • Proteomics of Synechocystis sp. strain PCC 6803
  • Signal peptidase I: cleaving the way to mature proteins
  • The Sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane
  • Targeting of lumenal proteins across the thylakoid membrane
  • The Tat system proofreads FeS protein substrates and directly initiates the disposal of rejected molecules
  • Localization of cytochrome b6f complexes implies an incomplete respiratory chain in cytoplasmic membranes of the cyanobacterium Synechocystis sp. PCC 6803
  • Surface display of small affinity proteins on Synechocystis sp. strain PCC 6803 mediated by fusion to the major type IV pilin PilA1
  • Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue
  • PaperBLAST: text mining papers for information about homologs
  • What’s in a name? the case of cyanobacteria
  • A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120
  • Appendages of the cyanobacterial cell
  • Localisation and interactions of the Vipp1 protein in cyanobacteria
  • Signal peptides for recombinant protein secretion in bacterial expression systems
  • Structure-function of cyanobacterial outer-membrane protein, Slr1270: homolog of Escherichia coli drug export/colicin import protein
  • Protein translocation and thylakoid biogenesis in cyanobacteria
  • Secretome analysis of Anabaena sp. PCC 7120 and the involvement of the TolC-homologue HgdD in protein secretion
  • Widespread distribution of cell defense against d-aminoacyl-tRNAs
  • The TolC-like protein HgdD of the cyanobacterium Anabaena sp. PCC 7120 is involved in secondary metabolite export and antibiotic resistance
  • Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins
  • A minimal Tat system from a gram-positive organism: a bifunctional TatA subunit participates in discrete TatAC and TatA complexes
  • Type I secretion systems – a story of appendices
  • Proteins in different Synechocystis compartments have distinguishing N-terminal features: a combined proteomics and multivariate sequence analysis
  • Localization of cytochrome b6f complexes implies an incomplete respiratory chain in cytoplasmic membranes of the cyanobacterium Synechocystis sp. PCC 6803
  • Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion
  • Type IV fimbrial biogenesis is required for protease secretion and natural transformation in Dichelobacter nodosus
  • Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP
  • Type I secretion in Gram-negative bacteria
  • MacSyFinder: a program to mine genomes for molecular systems with an application to CRISPR-Cas systems
  • From bacteria to chloroplasts: evolution of the chloroplast SRP system
  • Two minimal Tat translocases in Bacillus
  • Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria
  • Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway
  • Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion
  • Protein secretion through autotransporter and two-partner pathways
  • Evolutionary interplay between symbiotic relationships and patterns of signal peptide gain and loss
  • Efficient surface-display of autotransporter proteins in cyanobacteria
  • Identification of inner membrane translocase components of TolC-mediated secretion in the cyanobacterium Synechocystis sp. PCC 6803
  • The twin-arginine translocation (Tat) protein export pathway
  • Architecture, function, and substrates of the type II secretion system
  • A minimal Tat system from a gram-positive organism: a bifunctional TatA subunit participates in discrete TatAC and TatA complexes
  • Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803
  • Type I secretion in Gram-negative bacteria
  • The rich tapestry of bacterial protein translocation systems
  • Surface display of small affinity proteins on Synechocystis sp. strain PCC 6803 mediated by fusion to the major type IV pilin PilA1
  • Model for membrane organization and protein sorting in the cyanobacterium Synechocystis sp. PCC 6803 inferred from proteomics and multivariate sequence analyses
  • Probing Synechocystis-arsenic interactions through extracellular nanowires
  • Membrane-specific targeting of green fluorescent protein by the Tat pathway in the cyanobacterium Synechocystis PCC6803
  • SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins
  • TatE as a regular constituent of bacterial twin-arginine protein translocases
  • SecG is an auxiliary component of the protein export apparatus of Escherichia coli
  • The secretion signal peptide of the cyanobacterial extracellular protein HesF is located at its C-terminus
  • Axenic biofilm formation and aggregation by Synechocystis sp. strain PCC 6803 are induced by changes in nutrient concentration and require cell surface structures
  • A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane
  • Identification of inner membrane translocase components of TolC-mediated secretion in the cyanobacterium Synechocystis sp. PCC 6803
  • Enhancing CO2 bio-mitigation by genetic engineering of cyanobacteria
  • Structure-function of cyanobacterial outer-membrane protein, Slr1270: homolog of Escherichia coli drug export/colicin import protein
  • Identification of protein secretion systems in bacterial genomes
  • Factors controlling floc formation and structure in the cyanobacterium Synechocystis sp. PCC 6803
  • Appendages of the cyanobacterial cell
  • The Tat system proofreads FeS protein substrates and directly initiates the disposal of rejected molecules
  • Axenic biofilm formation and aggregation by Synechocystis sp. strain PCC 6803 are induced by changes in nutrient concentration and require cell surface structures
  • Evolutionary interplay between symbiotic relationships and patterns of signal peptide gain and loss
  • Structure of TatA paralog, TatE, suggests a structurally homogeneous form of Tat protein translocase that transports folded proteins of differing diameter
  • Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane
  • Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803
  • Cyanobacteria in motion
  • GDSL family of serine esterases/lipases
  • Cyanobacterial leader peptides for protein secretion
  • Recent advances in biological functions of thick pili in the cyanobacterium Synechocystis sp. PCC 6803
  • Tat‐dependent targeting of Rieske iron‐sulphur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC6803
  • Two-partner secretion: as simple as it sounds?
  • The plant mitochondrial TAT pathway is essential for complex III biogenesis
  • Proteomic analysis of the outer membrane of Anabaena sp. strain PCC 7120
  • Efficient surface-display of autotransporter proteins in cyanobacteria
  • Subcellular targeting by membrane lipids
  • Two-partner secretion: as simple as it sounds?
  • Heterogeneous Rieske proteins in the cytochrome b6f complex of Synechocystis PCC6803?
  • IM30 triggers membrane fusion in cyanobacteria and chloroplasts
  • Identification and characterization of the SecA protein homologue in the cyanobacterium Synechococcus PCC7942
  • Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli
  • Trimeric autotransporter adhesins: variable structure, common function
  • Plasmid conjugation from proteobacteria as evidence for the origin of xenologous genes in cyanobacteria
  • Model for membrane organization and protein sorting in the cyanobacterium Synechocystis sp. PCC 6803 inferred from proteomics and multivariate sequence analyses
  • Trimeric autotransporter adhesins: variable structure, common function
  • Two-partner secretion: combining efficiency and simplicity in the secretion of large proteins for bacteria-host and bacteria-bacteria interactions
  • Global proteomic analysis reveals an exclusive role of thylakoid membranes in bioenergetics of a model cyanobacterium
  • Type IV pili in Gram-positive bacteria
  • Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition
  • The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions
  • Protein translocation by the Sec61/Secy channel
  • Roles of DevBCA-like ABC transporters in the physiology of anabaena sp. PCC 7120
  • Export of complex cofactor-containing proteins by the bacterial Tat pathway
  • Type I protein secretion—deceptively simple yet with a wide range of mechanistic variability across the family
  • Protein targeting and translocation in cyanobacterial membrane biogenesis
  • Protein transport in organelles: protein transport into and across the thylakoid membrane: protein transport across thylakoid membranes
  • Proteomics of Synechocystis sp. strain PCC 6803
  • The twin-arginine translocation (Tat) protein export pathway
  • On the path to uncover the bacterial type II secretion system
  • Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae
  • Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway
  • Identification of protein secretion systems in bacterial genomes
  • Targeting of proteins to the twin-arginine translocation pathway
  • Structure and secretion of CofJ, a putative colonization factor of enterotoxigenic Escherichia coli
  • TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in Sec-independent protein export
  • Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane
  • PetC1 is the major Rieske iron-sulfur protein in the cytochrome b6f complex of Synechocystis sp. PCC 6803
  • Recent advances in biological functions of thick pili in the cyanobacterium Synechocystis sp. PCC 6803
  • The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains
  • Mutational analysis of genes involved in pilus structure, motility and transformation competency in the unicellular motile cyanobacterium Synechocystis sp. PCC6803
  • Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane
  • The TolC-like protein HgdD of the cyanobacterium Anabaena sp. PCC 7120 is involved in secondary metabolite export and antibiotic resistance
  • Endosymbiosis: did plastids evolve from a freshwater cyanobacterium?
  • Mutational analysis of genes involved in pilus structure, motility and transformation competency in the unicellular motile cyanobacterium Synechocystis sp. PCC6803
  • Developing Gram-negative bacteria for the secretion of heterologous proteins
  • Proteome mapping of a cyanobacterium reveals distinct compartment organization and cell-dispersed metabolism
  • Endosymbiosis: did plastids evolve from a freshwater cyanobacterium?
  • Protein translocation across the bacterial cytoplasmic membrane
  • Convergent evolution toward an improved growth rate and a reduced resistance range in Prochlorococcus strains resistant to phage
  • On the path to uncover the bacterial type II secretion system
  • Transfer of a genetic marker from a megaplasmid of Anabaena sp. strain PCC 7120 to a megaplasmid of a different Anabaena strain
  • Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey
  • Type IV pili-mediated secretion modulates Francisella virulence
  • Functional role of PilA in iron acquisition in the cyanobacterium Synechocystis sp. PCC 6803
  • Cyanobacteria in motion
  • Secretome analysis of Anabaena sp. PCC 7120 and the involvement of the TolC-homologue HgdD in protein secretion
  • Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility
  • Two minimal Tat translocases in Bacillus
  • Proteomic analysis of the outer membrane of Anabaena sp. strain PCC 7120
  • Roles of DevBCA-like ABC transporters in the physiology of anabaena sp. PCC 7120
  • TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in Sec-independent protein export
  • Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease
  • An expanded genomic representation of the phylum cyanobacteria
  • The bacterial twin-arginine translocation pathway
  • Targeting of lumenal proteins across the thylakoid membrane
  • The Tat protein export pathway and its role in cyanobacterial metalloprotein biosynthesis
  • Protein translocation across the bacterial cytoplasmic membrane
  • Plant mitochondria contain the protein translocase subunits TatB and TatC
  • Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803
  • Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria
  • Transfer of a genetic marker from a megaplasmid of Anabaena sp. strain PCC 7120 to a megaplasmid of a different Anabaena strain
  • Self-suppression of biofilm formation in the cyanobacterium Synechococcus elongatus
  • Protein export through the bacterial Sec pathway
  • What’s in a name? the case of cyanobacteria
  • Transport of folded proteins by the Tat system
  • Expression and secretion of a lytic polysaccharide monooxygenase by a fast-growing cyanobacterium
  • Export of complex cofactor-containing proteins by the bacterial Tat pathway
  • Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease
  • Self-suppression of biofilm formation in the cyanobacterium Synechococcus elongatus
  • SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins
  • Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility
  • A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120
  • The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC6803
  • mRNA localisation, reaction centre biogenesis and thylakoid membrane targeting in cyanobacteria
  • Global proteomic analysis reveals an exclusive role of thylakoid membranes in bioenergetics of a model cyanobacterium
  • Chapter 18 - cyanobacterial secretion systems: understanding fundamental mechanisms toward technological applications
  • Protein targeting, transport and translocation in cyanobacteria
  • SecG is an auxiliary component of the protein export apparatus of Escherichia coli
  • The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains
  • Signal peptidase I: cleaving the way to mature proteins
  • Heterologous expression of mlrA in a photoautotrophic host – engineering cyanobacteria to degrade microcystins
  • Protein translocation by the Sec61/Secy channel
  • Probing Synechocystis-arsenic interactions through extracellular nanowires
  • Type IV pili-mediated secretion modulates Francisella virulence
  • Structure and secretion of CofJ, a putative colonization factor of enterotoxigenic Escherichia coli
  • Protein export through the bacterial Sec pathway
  • Subcellular targeting by membrane lipids
  • The versatile TolC-like Slr1270 in the cyanobacterium Synechocystis sp. PCC 6803
  • PaperBLAST: text mining papers for information about homologs
  • The Tat protein export pathway and its role in cyanobacterial metalloprotein biosynthesis
  • Identification and characterization of the SecA protein homologue in the cyanobacterium Synechococcus PCC7942
  • MacSyFinder: a program to mine genomes for molecular systems with an application to CRISPR-Cas systems
  • Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane
  • PetC1 is the major Rieske iron-sulfur protein in the cytochrome b6f complex of Synechocystis sp. PCC 6803
  • Proteins in different Synechocystis compartments have distinguishing N-terminal features: a combined proteomics and multivariate sequence analysis
  • Convergent evolution toward an improved growth rate and a reduced resistance range in Prochlorococcus strains resistant to phage
  • Expression and secretion of a lytic polysaccharide monooxygenase by a fast-growing cyanobacterium
  • Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway
  • Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue
  • Heterologous expression of mlrA in a photoautotrophic host – engineering cyanobacteria to degrade microcystins
  • Genomic structure of an economically important cyanobacterium, Arthrospira (Spirulina) platensis NIES-39
  • The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120
  • HesF, an exoprotein required for filament adhesion and aggregation in Anabaena sp. PCC 7120
  • Plant mitochondria contain the protein translocase subunits TatB and TatC
  • Plasmid conjugation from proteobacteria as evidence for the origin of xenologous genes in cyanobacteria
  • Cyanobacterial leader peptides for protein secretion
  • Widespread distribution of cell defense against d-aminoacyl-tRNAs
  • Type IV pili in Gram-positive bacteria
  • The secretion signal peptide of the cyanobacterial extracellular protein HesF is located at its C-terminus
  • The bacterial twin-arginine translocation pathway
  • Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803
  • Inactivation of a predicted leader peptidase prevents photoautotrophic growth of Synechocystis sp. strain PCC 6803
  • The versatile TolC-like Slr1270 in the cyanobacterium Synechocystis sp. PCC 6803
  • Protein targeting and translocation in cyanobacterial membrane biogenesis
  • Proteome mapping of a cyanobacterium reveals distinct compartment organization and cell-dispersed metabolism
  • The rich tapestry of bacterial protein translocation systems
  • Two-partner secretion: combining efficiency and simplicity in the secretion of large proteins for bacteria-host and bacteria-bacteria interactions
  • Protein transport in organelles: protein transport into and across the thylakoid membrane: protein transport across thylakoid membranes
  • TatE as a regular constituent of bacterial twin-arginine protein translocases
  • Tat‐dependent targeting of Rieske iron‐sulphur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC6803
  • Localisation and interactions of the Vipp1 protein in cyanobacteria
  • Chapter 18 - cyanobacterial secretion systems: understanding fundamental mechanisms toward technological applications
  • Type I secretion systems – a story of appendices
  • Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803
  • Small secreted proteins enable biofilm development in the cyanobacterium Synechococcus elongatus
  • Targeting of proteins to the twin-arginine translocation pathway
  • Type I protein secretion—deceptively simple yet with a wide range of mechanistic variability across the family
  • An expanded genomic representation of the phylum cyanobacteria
  • Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway
  • A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane
  • Extracellular proteins: novel key components of metal resistance in cyanobacteria?
  • Protein targeting, transport and translocation in cyanobacteria
  • The plant mitochondrial TAT pathway is essential for complex III biogenesis
  • Enhancing CO2 bio-mitigation by genetic engineering of cyanobacteria
  • Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae
  • Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP
  • The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions
  • Heterogeneous Rieske proteins in the cytochrome b6f complex of Synechocystis PCC6803?
  • Type IV fimbrial biogenesis is required for protease secretion and natural transformation in Dichelobacter nodosus
  • Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition
  • The Sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane
  • The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC6803
  • Structure of TatA paralog, TatE, suggests a structurally homogeneous form of Tat protein translocase that transports folded proteins of differing diameter
  • Small secreted proteins enable biofilm development in the cyanobacterium Synechococcus elongatus