Ribosomes: The New Role of Ribosomal Proteins as Natural Antimicrobials
Abstract
:1. Introduction
2. Ribosome
2.1. Composition
2.2. Nomenclature
Ribosomes Proteins of the Small Subunit | ||||||||
Family Name | Alt. Name 1 | Taxonomic Range | Univ. Cons. 2 | Deleted Mutant | Ribosomal Function/Comment | |||
A | B | E | O | |||||
bS1 | ○ | ● | ○ | C | X | Brings with mRNA into the proximity of the ribosome during initiation; involvement in translational regulation [16,17,18] | ||
uS2 | S0Ae | ● | ● | ● | C, M | 1 | Involvement in translational regulation [17] | |
uS3 | S3e | ● | ● | ● | C, M | 1 | Forms the mRNA entry pore and may exhibit helicase activity to unwind mRNA secondary structures encountered during translation [18] | |
uS4 | S9e | ● | ● | ● | C | Mutations (ram) increase the error during the decoding process; with uS7 as one of the two assembly initiator proteins; involvement in translational regulation [16,17,18] | ||
uS5 | S2e | ● | ● | ● | C, M, T | 1 | Probably facilitates changes in rRNA conformation that alter the selection mode of the ribosome from accurate to error-prone and vice versa [16,17,18] | |
bS6 | ○ | ● | ○ | C, M, T | X | Form a tight complex that assembles as a heterodimer on the outer edge of the platform of the subunits [16] | ||
uS7 | S5e | ● | ● | ● | C, M | 1 | mRNA and tRNA binding at the E site; involvement in translational regulation [16,17,19] | |
uS8 | S22e | ● | ● | ● | C, T | 1 | Involvement in translational regulation [17] | |
uS9 | S16e | ● | ● | ● | C, M, T | 1 | X | Interaction with P site [19] |
uS10 | S20e | ● | ● | ● | C, M | 1 | uS3, uS10, and uS14 form a tight protein cluster at the back of the 30S head [16] | |
uS11 | S14e | ● | ● | ● | C, M, T | 1 | X | Forms part of the binding site of the anticodon loop of E-tRNA [19] |
uS12 | S23e | ● | ● | ● | C, M | 1 | Involved in decoding of the coding of the second and third codon positions at the A site [16,17,18,19] | |
uS13 | S18e | ● | ● | ● | C | X | Interaction with P site tRNA [19] | |
uS14 | S29e | ● | ● | ● | C, M | 1 | uS3, uS10, and uS14 form a tight protein cluster at the back of the 30S head [16] | |
uS15 | S13e | ● | ● | ● | C, M, T | 1 | Involvement in translational regulation [17] | |
bS16 | ○ | ● | ○ | C, M, T | Improve the stability of ribosome [16] | |||
uS17 | S11e | ● | ● | ● | C, M, T | 1 | X | Ribosome assembly [20] |
bS18 | ○ | ● | ○ | C, M, T | Form a tight complex that assembles as heterodimer on the outer edge of the platform [16] | |||
uS19 | S15e | ● | ● | ● | C | Inter-subunit bridges; related to the changes in the information between LSU and SSU [20] | ||
bS20 | ○ | ● | ○ | C | X | Involvement in translational regulation [17] | ||
bS21 | ○ | ● | ○ | M | Required for the recognition of native templates; stabilize the ribosome [21] | |||
bS22 | ○ | ● | ○ | ○ | Accumulates in ribosomes of the stationary phase, so is a factor rather than an RP [17] | |||
bTHX | ○ | ● | ○ | ○ | Found in thermophilic bacteria and stabilizes the organization of RNA elements at the 30S subunit [21] | |||
eS1 | ● | ○ | ● | ○ | Initiation of translation by catching the mRNA and directing it to the ribosome; involvement in translational regulation [17,18] | |||
eS4 | ● | ○ | ● | ○ | Assembly initiator protein; involvement in translational regulation [16,17] | |||
eS6 | ● | ○ | ● | ○ | Form a tight complex that assembles as heterodimer on the outer edge of the platform [16] | |||
eS7 | ○ | ○ | ● | ○ | mRNA and tRNA binding at the E site; involvement in translational regulation [16,19] | |||
eS8 | ● | ○ | ● | ○ | Involvement in translational regulation [17] | |||
eS10 | ○ | ○ | ● | ○ | Associated ribosome quality control; stall translation on poly(A) sequences [22] | |||
eS12 | ○ | ○ | ● | ○ | tRNA decoding at the A site [19] | |||
eS17 | ● | ○ | ● | ○ | Ribosome assembly [20] | |||
eS19 | ● | ○ | ● | ○ | Inter-subunit bridges [20] | |||
eS21 | ○ | ○ | ● | ○ | Required for the recognition of native templates and its function resembles the function of bS1 [21] | |||
eS24 | ● | ○ | ● | ○ | Required for processing of pre-RNA and maturation of SSU [23] | |||
eS25 | ● | ○ | ● | ○ | Translation of mRNAs from specific cellular pathways [24] | |||
eS26 | ○ | ○ | ● | ○ | Involved in the formation of the mRNA binding channel in the region of the exit site [25] | |||
eS27 | ● | ○ | ● | ○ | Fused to C-terminus of ubiquitin; zinc finger [4] | |||
eS28 | ● | ○ | ● | ○ | mRNA interactions [4] | |||
eS30 | ● | ○ | ● | ○ | Replaces part of bS4 [4] | |||
eS31 | ● | ○ | ● | ○ | Ribosome assembly [26] | |||
RACK1 | ○ | ○ | ● | ○ | Interacts with signaling molecules; through this interaction, the regulation of translation is mediated [18,19] | |||
Ribosomal Proteins of the Large Subunit | ||||||||
Family Name | Alt. Name 1 | Taxonomic Range | Univ. Cons. 2 | Deleted Mutant | Ribosomal Function/Comment | |||
A | B | E | O | |||||
uL1 | L10a | ● | ● | ● | C, M | 1 | X | Possibly involved in the disposal of deacylated tRNA that has been release from the E site; translational feedback regulation of L11 operon; involvement in translational regulation [16,17,18] |
uL2 | L2e | ● | ● | ● | C, M, T | 1 | Residue histidine 229 is possibly involved in the peptidyltransferase reaction [17,19] | |
uL3 | L3e | ● | ● | ● | C, M, T | 1 | Assembly initiation: forms an assembly starting point at the 3’region of 23S rRNA of the LSU; plays a role in the allosteric coordination of the peptidyl transferase center (PTC) [16,17,19] | |
uL4 | L4e | ● | ● | ● | C, M, T | 1 | Role in rRNA transcription antitermination; involvement in translational regulation [16,17,18] | |
uL5 | L11e | ● | ● | ● | C | With uS13, forms different contacts in the rotational states of ribosome; interaction with P site tRNA [19] | ||
uL6 | L9e | ● | ● | ● | C | Forms the factor-binding site at the edge of the inter-subunit cleft of the ribosome [19] | ||
bL9 | ○ | ● | ○ | C, M, T | Mutations might affect the precise arrangement of a tRNA in the P site [17,18] | |||
uL10 | P0 | ● | ● | ● | M | Involvement in translational regulation [17,19] | ||
uL11 | L12e | ● | ● | ● | C, M, T | 1 | X | During the stringent response, L11 senses the presence of a deacylated tRNA in the A site [16,17,18] |
bL12 | ○ | ● | ○ | C, M | Involved in elongation-factor binding, possibly in GTPase activation and in translational regulation [16,17,18] | |||
uL13 | L16e | ● | ● | ● | C, M, T | 1 | Can repress rRNA transcription termination [27] | |
uL14 | L23e | ● | ● | ● | C, M, T | 1 | Forms the factor-binding site at the edge of the inter-subunit cleft of the ribosome [19] | |
uL15 | L28e | ● | ● | ● | M, T | X | Essential late assembly step that is important for an active ribosomal conformation; improve the stability of ribosomes [16,17] | |
uL16 | L10e | ● | ● | ● | C, M, T | 1 | Essential late assembly step. May be involved in correct positioning of the acceptor stem of A and P site tRNA as well as ribosome recycling factor (RRF) on the ribosome; acts in information transmission of the eukaryotic ribosome [16,17,18,26] | |
bL17 | ○ | ● | ○ | M, T | Forms a ring around the tunnel exit site [18] | |||
uL18 | L5e | ● | ● | ● | C, M | 1 | With L5 and L25, forms a complex with 5S rRNA which constitutes the central protuberance of the SSU [17] | |
bL19 | ○ | ● | ○ | C, M | X | Inter-subunit bridge in the ribosome [20] | ||
bL20 | ○ | ● | ○ | C, M, T | Involvement in translational regulation; improve the stability of ribosomes [17] | |||
bL21 | ○ | ● | ○ | C, M, T | Direct contact with the 23S rRNA [26,28] | |||
uL22 | L17e | ● | ● | ● | C, M, T | 1 | May interact with specific nascent chains to regulate translation [16,17,18] | |
uL23 | L25e | ● | ● | ● | C, M, T | 1 | Present at the tunnel exit site and has been shown to be a component of the chaperone trigger factor binding site on the ribosome [16,18] | |
uL24 | L26e | ● | ● | ● | C, M, T | 1 | X | Important for assembly initiation; improve the stability of ribosomes [16,17] |
bL25 | ○ | ● | ○ | ○ | With L5 and L18 forms a complex with 5S rRNA, that constitutes the central protuberance of the SSU [17] | |||
bL27 | ○ | ● | ○ | C, M, T | X | Implicated in the placement of the acceptor stem of P site binding of the ribosome recycling factor on the 50S subunit [16,18] | ||
bL28 | ○ | ● | ○ | C, M, T | X | Assembly protein [20] | ||
uL29 | L35e | ● | ● | ● | C, M, T | 1 | X | Located close to the tunnel exit site and may constitute part of the binding site for the signal recognition particle [16,18,26] |
uL30 | L7e | ● | ● | ● | M, T | X | Assembly of the bacterial SSU or the eukaryotic LSU [26] | |
bL31 | ○ | ● | ○ | C | Contributes to ribosome subunit association [20,28,29] | |||
bL32 | ○ | ● | ○ | C, M | Forms part of the tunnel near to the peptidyl transferase center [18] | |||
bL33 | ○ | ● | ○ | C, M, T | X | Assembly protein [20] | ||
bL34 | ○ | ● | ○ | ○ | Ribosome-constituting protein [30] | |||
bL35 | ○ | ● | ○ | C, M | Assembly protein [20] | |||
bL36 | ○ | ● | ○ | C, M | Assembly protein [20] | |||
P1/P2 | ● | ○ | ● | ○ | Mediate elongation factor GTPase activity [16] | |||
eL6 | ○ | ○ | ● | ○ | Part of the peptidyl transferase center [20] | |||
eL8 | L7a | ● | ○ | ● | ○ | Assembly of the bacterial SSU or the eukaryotic LSU [26] | ||
eL13 | ● | ○ | ● | ○ | Can repress rRNA transcription termination; forms bridges between LSU and SSU [15] | |||
eL14 | ● | ○ | ● | ○ | Role in GAC; forms part from the elongation factors to the mRNA exit tunnel [20] | |||
eL15 | ● | ○ | ● | ○ | Improves the stability of ribosomes [16,17] | |||
eL18 | ● | ○ | ● | ○ | Forms tetrameric complex with 5S rRNA [17] | |||
eL19 | ● | ○ | ● | ○ | Peptide exit tunnel; participates in inter-subunit bridges [20,26], | |||
eL20 | ○ | ○ | ● | ○ | Improves the stability of ribosomes [16] | |||
eL21 | ● | ○ | ● | ○ | Bridges functional sites: peptidyl transferase center, the tunnel, and a tRNA binding site [26] | |||
eL22 | ○ | ○ | ● | ○ | Ribosome assembly and protein translation [16,19] | |||
eL24 | L10a | ● | ○ | ● | ○ | Improves the stability of ribosomes [17] | ||
eL27 | ○ | ○ | ● | ○ | Binding of tRNA to the ribosome [16] | |||
eL28 | ○ | ○ | ● | ○ | Assembly protein [20] | |||
eL29 | ○ | ○ | ● | ○ | Assembly of the SSU [26] | |||
eL30 | ● | ○ | ● | ○ | Assembly of the SSU [26] | |||
eL31 | ● | ○ | ● | ○ | Contributes to ribosome subunit association [29] | |||
eL32 | ● | ○ | ● | ○ | Forms part of the tunnel exit site [18] | |||
eL33 | ● | ○ | ● | ○ | Assembly protein; interacts directly with E site tRNA [20,28] | |||
eL34 | ● | ○ | ● | ○ | Ribosome-constituting protein [30] | |||
eL36 | ○ | ○ | ● | ○ | Assembly protein [20] | |||
eL37 | ● | ○ | ● | ○ | Structural constituent of ribosome; binds to the 23S rRNA [28] | |||
eL38 | ● | ○ | ● | ○ | Subunit of the cytosolic LSU; involved in translation [31] | |||
eL39 | ● | ○ | ● | ○ | Lines the tunnel and gives it its own “Teflon-like” properties [19] | |||
eL40 | ● | ○ | ● | ○ | Enables protein binding and ubiquitin protein ligase binding [32] | |||
eL41 | ● | ○ | ● | ○ | Interacts with beta subunit of protein kinase CKII and stimulates phosphorylation of DNA topoisomerase [33] | |||
eL42 | L44a | ● | ○ | ● | ○ | Enables RNA binding and structural constituent of ribosome [34] | ||
eL43 | L37Ae | ● | ○ | ● | ○ | Enables RNA binding and structural constituent of ribosome [35] |
2.3. Structure
2.4. Role of Ribosomes in the Cell Translation Process
3. Moonlighting Proteins
Ribosomal Proteins as Moonlighting Proteins
Ribosomal Protein as AMP | Peptide Sequence | Isolated From | Against Microorganism | Physiochemical Properties | ||
---|---|---|---|---|---|---|
Hydrophobic | Iso-Electric Point (pH) | Net Charge at pH 7 | ||||
RP eS30 6.6 kDa [54] | KVHGSLARAGK | Oncorhynchus mykiss | P. citreus and Bacillus subtilis | 36.36% | 11.57 | 3.1 |
RP bS21 6.7 kDa [57] | GKTVVRSNESLDDALRRFKRSVSKAGTIQEYRKR | L. sakei | Enterococcus faecalis, L. sakei, L. innocua, L. monocytogenes, Listeria seeligeri, and Staphylococcus epidermidis | 29.41% | 11.31 | 6 |
RP uL1 24.6 kDa [65] | ---- | Lactobacillus Hma2N | Melissococcus plutonius | ---- | ---- | ---- |
RP eL29 6.4 kDa [66] | AKSKNHTSHNQNRKQHRNGIHRPKTYRYPSMKGVDPKFLKNLKFSKKHNKNTKK | Crassostrea gigas | B. subtilis, E. coli and Vibrio parahaemolyticus | 18.52% | 11.71 | 16.5 |
RP bL27 9.9 kDa [58] | ---- | L. salivarius | S. pyogenes, S. uberis, and E. faecium | ---- | ---- | ---- |
RP bL36 4.4 kDa [60] | MKVRPSVKPMCEHCKIIKRKGRVMVICSANPKHKQRQGK | P. acidilactici OSU-PECh-3A | E. coli | 35.9% | 11.3 | 11 |
RP eL27 4.1 kDa [67] | PALKRKARREAKVKFEXRYXTGXNXXFFQ | Silurus asotus | B. subtilis, S. aureus, Micrococcus luteus, and Streptococcus iniae | 37.5% | 11.3 | 11 |
RP uL1 15 kDa [61] | ---- | B. tequilensis | S. aureus | ---- | ---- | ---- |
Peptide | Peptide Sequence 1 | Reference Organism | Against Microorganism | Physiochemical Properties | ||
---|---|---|---|---|---|---|
Hydrophobic | Iso-Electric Point (pH) | Net Charge at pH 7 | ||||
RP uL1 (2–20) [53] | ---- | H. pylori | E. coli | ---- | ---- | ---- |
RP uL1 HP-A3 (A3-NT) [72] | FKRLEKLFSKIWNWK-NH2 | H. pylori | C. albicans, Trichosporn beigelii, and Saccharomyces cerevisiae | 46.67% | 11.3 | 11 |
RP uL1 (F1A) [73] | AKRLKKLFKKIWNWK-NH2 | H. pylori | E. coli, Pseudomonas aeruginosa, Proteus vulgaris, Salmonella typhimurium, S. aureus, L. monocytogenes, S. epidermidis, C. albicans, T. beigelii, Aspergillus awamori, Aspergillus flavus, Aspergillus fumigatus, and Aspergillus parasiticus | 46.67% | 11.86 | 7 |
RP uL1 (F8A) [73] | FKRLKKLAKKIWNWK-NH2 | 46.67% | 11.86 | 7 | ||
RP uL1 (F1AF8A) [73] | AKRLKKLAKKIWNWK-NH2 | 46.67% | 11.86 | 7 | ||
RP uL1 (A2) [73] | AKRLKKLAKKIWKWK-NH2 | 46.67% | 11.91 | 8 | ||
RP eL39 (PaDBS1R1) 2.1 kDa [74] | PKILNKILGKILRLAAAFK | Pyrobaculum aerophilum | Klebsiella pneumoniae and S. aureus | 57.89% | 11.79 | 5 |
RP S23 (BjRPS23 67–84) 15.8 kDa [75] | MGKPRGLRSARKLKDHRRQQRWHDKSFKKAHLGTAVKASPFGGASHAKGIVLEKIGVEAKQPNSAIRKCVRVQLIKNGKKITAFVPNDGCLNYIEENDEVLVSGFGRKGRAVGDIPGVRFKVVKVANVSLLALFKEKKERPRS | B. japonicum | E. coli, A. hydrophila, S. aureus, and M. luteus | 37.76% | 11.22 | 21.3 |
RP S23 (BjRPS23 17–38) 2.6 kDa [75] | RRQQRWHDKSFKKAHLGTAVKA | S. aureus | 31.82% | 11.93 | 6.2 | |
RP S23 (BjRPS23 67–84) 2.1 kDa [75] | RKCVRVQLIKNGKKITAF | E. coli, A. hydrophila, S. aureus, and M. luteus | 44.44% | 11.57 | 5.9 | |
RP uS15 16.9 kDa [1] | MADEQAALKKKRTFRKYTYRGVDLDQLLDMSSEQLMEMMKARPRRRFSRGLKRKHLALIKKLRKAKKECPALEKPEVVKTHLRNTVIVPEMIGSIVAVYNGKTFNQVEVKPEMIGHYLGEFSITYKPVKHGRPGIGATHSSRFIPLK | B. japonicum | A. hydrophila, E. coli, S. aureus, and B. subtilis | 39.46% | 10.82 | 18.4 |
RP uS15 (45–67) [1] | RRFSRGLKRKHLALIKKLRKAKK | 34.78% | 12.73 | 12.1 | ||
RP eL30 12.7 kDa [2] | ---- | B. japonicum | A. hydrophila and S. aureus | ---- | ---- | ---- |
RP eL30 (2–27) [2] | KQKRKTMESINSRLQLVMKSGKYVLG | 34.62% | 11.2 | 6 | ||
RP eL30 (23–46) [2] | KYVLGLKETLKVLRQGKAKLIIIA | 54.17% | 10.88 | 5 | ||
RP bS1 (V10I) 1.1 kDa [76] | VTDFGVFVEI | Thermus thermophilus | T. thermophilus | 60% | 0.66 | −2 |
RP bS1 (R23I) 2.6 kDa [76] | RKKRRQRRRGGSar#(A)GVTDFGVFVEI | 30.77% | 12.24 | 7 | ||
RP bS1 (R23T) 2.5 kDa [76] | RKKRRQRRRGGSar#(A)GVVEGTVVEVT | 26.92% | 12.24 | 7 | ||
RP bS1 [77] | ---- | T. thermophilus | P. aeruginosa | ---- | ---- | ---- |
RP bS1 (R23R) 2.8 kDa [78] | RKKRRQRRRGGGGLHITDMAWKR | P. aeruginosa | P. aeruginosa | 21.74% | 12.51 | 9.1 |
RP bS1 (R23L) 2.6 kDa [78] | RKKRRQRRRGGGGITDFGIFIGL | 26.09% | 12.41 | 7 | ||
RP bS1 (R23F) [79] | RKKRRQRRRGGSarGVVVHI-Asi-GGKF-NH2 | S. aureus | S. aureus, P. aeruginosa, E. coli, and Bacillus cereus | 29.63% | 12.89 | 10.1 |
RP bS1 (R2DI) [79] | RKKRRQRRRGGSarGLTQFGAFIDI-NH2 | 28% | 12.51 | 8 | ||
RP bS1 (R23EI) [79] | RKKRRQRRRGGSarGVQGLVHISEI-NH2 | 24% | 12.51 | 8.1 |
4. Applications of AMPs
5. Possible RP Mechanism of Action as AMPs
6. Future Developments and Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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DOMAIN | |||
---|---|---|---|
Bacteria | Eukarya | Archaea | |
Ribosome | 70S | 80S | 70S |
Molecular mass | 2.3 MDa | ~4.5 MDa | ~4.5 MDa |
Large subunit (LSU) | 50S | 60S | 50S |
rRNA | 23S, 5S | 5.8S, 25–28S, 5S | 23S, 5S |
Number of proteins | 33 | 46 | 40 |
Small subunit (SSU) | 30S | 40S | 30S |
rRNA | 16S | 18S | 16S |
Number of proteins | 21 | 32 | 28 |
Database | Website |
---|---|
MoonProt | http://www.moonlightingproteins.org |
Multitasking Proteins DataBase | http://wallace.uab.es/multitaskII |
MultitaskProtDB-II | http://moondb.hb.univ-amu.fr |
PlantMP | https://www.plantmp.com |
AMP | Application | Route of Administration |
---|---|---|
Dalbavancin, oritavancin, and telavancin | Complicated skin infections | Intravenous infusion |
Vancomycin | Against Gram-positive bacteria Treats diarrhea associated with Clostridium difficile, pseudomembranous colitis, and infection | Intravenous infusion |
Bacitracin | Skin and eye infections | Intramuscular |
Polymyxin E (colistins) | Gastrointestinal tract infections caused by E. coli and Salmonella spp. | Intramuscular or intravenous |
Polymyxin B | Last-line treatment alternative for resistant Gram-negative bacterial infections | Intramuscular, intravenous, intrathecal ophthalmic |
Tyrothricin | Treatment of infected skin and oropharyngeal mucous membranes Effective against Gram-positive bacteria | Topical application only |
Gramicidin D (or just gramicidin) | Skin lesions, surface wounds, and eye infections | External use only |
Gramicidin S | Against Gram-negative and Gram-positive bacteria and fungi Used to treat genital ulcers caused by sexually transmitted diseases | Topical application only |
Daptomycin | Skin infections caused by Gram-positive bacteria | Intravenous injection |
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Hurtado-Rios, J.J.; Carrasco-Navarro, U.; Almanza-Pérez, J.C.; Ponce-Alquicira, E. Ribosomes: The New Role of Ribosomal Proteins as Natural Antimicrobials. Int. J. Mol. Sci. 2022, 23, 9123. https://doi.org/10.3390/ijms23169123
Hurtado-Rios JJ, Carrasco-Navarro U, Almanza-Pérez JC, Ponce-Alquicira E. Ribosomes: The New Role of Ribosomal Proteins as Natural Antimicrobials. International Journal of Molecular Sciences. 2022; 23(16):9123. https://doi.org/10.3390/ijms23169123
Chicago/Turabian StyleHurtado-Rios, Jessica J., Ulises Carrasco-Navarro, Julio Cesar Almanza-Pérez, and Edith Ponce-Alquicira. 2022. "Ribosomes: The New Role of Ribosomal Proteins as Natural Antimicrobials" International Journal of Molecular Sciences 23, no. 16: 9123. https://doi.org/10.3390/ijms23169123