Sequence and evolutionary analysis of bacterial ribosomal S1 proteins.
S1 server
evolutionary analysis
residue conservation
ribosomal S1 proteins
Journal
Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
17
03
2021
received:
18
11
2020
accepted:
07
04
2021
pubmed:
13
4
2021
medline:
5
2
2022
entrez:
12
4
2021
Statut:
ppublish
Résumé
The multi-domain bacterial S1 protein is the largest and most functionally important ribosomal protein of the 30S subunit, which interacts with both mRNA and proteins. The family of ribosomal S1 proteins differs in the classical sense from a protein with tandem repeats and has a "bead-on-string" organization, where each repeat is folded into a globular domain. Based on our recent data, the study of evolutionary relationships for the bacterial phyla will provide evidence for one of the proposed theories of the evolutionary development of proteins with structural repeats: from multiple repeats of assembles to single repeats, or vice versa. In this comparative analysis of 1333 S1 sequences that were identified in 24 different phyla, we demonstrate how such phyla can form independently/dependently during evolution. To the best of our knowledge, this work is the first study of the evolutionary history of bacterial ribosomal S1 proteins. The collected and structured data can be useful to computer biologists as a resource for determining percent identity, amino acid composition and logo motifs, as well as dN/dS ratio in bacterial S1 protein. The obtained research data indicate that the evolutionary development of bacterial ribosomal S1 proteins evolved from multiple assemblies to single repeat. The presented data are integrated into the server, which can be accessed at http://oka.protres.ru:4200.
Substances chimiques
Ribosomal Proteins
0
ribosomal protein S1
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1111-1124Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Yutin N, Puigbò P, Koonin EV, Wolf YI. Phylogenomics of prokaryotic ribosomal proteins. PLoS One. 2012;7(5):e36972. https://doi.org/10.1371/journal.pone.0036972.
Pilla SP, Bahadur RP. Residue conservation elucidates the evolution of r-proteins in ribosomal assembly and function. Int J Biol Macromol. 2019;140:323-329. https://doi.org/10.1016/j.ijbiomac.2019.08.127.
Roberts E, Sethi A, Montoya J, Woese CR, Luthey-Schulten Z. Molecular signatures of ribosomal evolution. Proc Natl Acad Sci U S A. 2008;105(37):13953-13958. https://doi.org/10.1073/pnas.0804861105.
Lecompte O, Ripp R, Thierry J-C, Moras D, Poch O. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 2002;30(24):5382-5390. https://doi.org/10.1093/nar/gkf693.
Ramulu HG, Groussin M, Talla E, Planel R, Daubin V, Brochier-Armanet C. Ribosomal proteins: toward a next generation standard for prokaryotic systematics? Mol Phylogenet Evol. 2014;75(1):103-117. https://doi.org/10.1016/j.ympev.2014.02.013.
Machulin A, Deryusheva E, Lobanov M, Galzitskaya O. Repeats in S1 proteins: flexibility and tendency for intrinsic disorder. Int J Mol Sci. 2019;20(10):2377. https://doi.org/10.3390/ijms20102377.
Deryusheva EI, Machulin AV, Matyunin MA, Galzitskaya OV. Investigation of the relationship between the S1 domain and its molecular functions derived from studies of the tertiary structure. Molecules. 2019;24(20):3681. https://doi.org/10.3390/molecules24203681.
Deryusheva EI, Machulin AV, Selivanova OM, Galzitskaya OV. Taxonomic distribution, repeats, and functions of the S1 domain-containing proteins as members of the OB-fold family. Proteins. 2017;85(4):602-613. https://doi.org/10.1002/prot.25237.
Machulin AV, Deryusheva EI, Selivanova OM, Galzitskaya OV. The number of domains in the ribosomal protein S1 as a hallmark of the phylogenetic grouping of bacteria. PLoS One. 2019;14(8):e0221370. https://doi.org/10.1371/journal.pone.0221370.
Sørensen MA, Fricke J, Pedersen S. Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J Mol Biol. 1998;280(4):561-569. https://doi.org/10.1006/jmbi.1998.1909.
Okada T, Wower IK, Wower J, Zwieb CW, Kimura M. Contribution of the second OB fold of ribosomal protein S1 from Escherichia coli to the recognition of tmRNA. Biosci Biotechnol Biochem. 2004;68(11):2319-2325. https://doi.org/10.1271/bbb.68.2319.
Skouv J, Schnier J, Rasmussen MD, Subramanian AR, Pedersen S. Ribosomal protein S1 of Escherichia coli is the effector for the regulation of its own synthesis. J Biol Chem. 1990;265(28):17044-17049.
Subramanian AR. Structure and functions of ribosomal protein S1. Prog Nucleic Acid Res Mol Biol. 1983;28:101-142.
Boni IV, Artamonova VS, Dreyfus M. The last RNA-binding repeat of the Escherichia coli ribosomal protein S1 is specifically involved in autogenous control. J Bacteriol. 2000;182(20):5872-5879. https://doi.org/10.1128/JB.182.20.5872-5879.2000.
Guerrier-Takada C, Subramanian AR, Cole PE. The activity of discrete fragments of ribosomal protein S1 in Q beta replicase function. J Biol Chem. 1983;258(22):13649-13652.
Bisaglia M, Laalami S, Uzan M, Bontems F. Activation of the RegB endoribonuclease by the S1 ribosomal protein is due to cooperation between the S1 four C-terminal modules in a substrate-dependant manner. J Biol Chem. 2003;278(17):15261-15271. https://doi.org/10.1074/jbc.M212731200.
Salah P, Bisaglia M, Aliprandi P, Uzan M, Sizun C, Bontems F. Probing the relationship between gram-negative and gram-positive S1 proteins by sequence analysis. Nucleic Acids Res. 2009;37(16):5578-5588. https://doi.org/10.1093/nar/gkp547.
Deryusheva EI, Selivanova OM, Serdyuk IN. Loops and repeats in proteins as footprints of molecular evolution. Biochemistry (Mosc). 2012;77(13):1487-1499. https://doi.org/10.1134/S000629791213007X.
Duan H, Liu G, Wang X, et al. Evaluation of the ribosomal protein S1 gene (rpsA) as a novel biomarker for mycobacterium species identification. Biomed Res Int. 2015;2015:271728-271728. https://doi.org/10.1155/2015/271728.
Cock PJA, Antao T, Chang JT, et al. Biopython: freely available python tools for computational molecular biology and bioinformatics. Bioinformatics. 2009;25(11):1422-1423. https://doi.org/10.1093/bioinformatics/btp163.
Mukherjee S, Stamatis D, Bertsch J, et al. Genomes Online database (GOLD) v.7: updates and new features. Nucleic Acids Res. 2019;47(D1):D649-D659. https://doi.org/10.1093/nar/gky977.
Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2018;46(D1):D493-D496. https://doi.org/10.1093/nar/gkx922.
Bateman A, Martin MJ, O'Donovan C, et al. UniProt: a hub for protein information. Nucleic Acids Res. 2015;43(D1):D204-D212. https://doi.org/10.1093/nar/gku989.
Crooks GE, Hon G, Chandonia J-M, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188-1190. https://doi.org/10.1101/gr.849004.
Goldman N, Yang Z. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 1994;11(5):725-736. https://doi.org/10.1093/oxfordjournals.molbev.a040153.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547-1549. https://doi.org/10.1093/molbev/msy096.
Ludwig W, Klenk H-P. Overview: A phylogenetic backbone and taxonomic framework for procaryotic systematics. Bergey's Manual® of Systematic Bacteriology. New York: Springer; 2001:49-65. https://doi.org/10.1007/978-0-387-21609-6_8.
Gupta RS. The phylogeny and signature sequences characteristics of fibrobacteres, chlorobi, and bacteroidetes. Crit Rev Microbiol. 2004;30(2):123-143. https://doi.org/10.1080/10408410490435133.
Gupta RS, Bhandari V, Naushad HS. Molecular signatures for the PVC clade (planctomycetes, verrucomicrobia, chlamydiae, and lentisphaerae) of bacteria provide insights into their evolutionary relationships. Front Microbiol. 2012;3:327. https://doi.org/10.3389/fmicb.2012.00327.
Battistuzzi FU, Feijao A, Hedges SB. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol. 2004;4:44. https://doi.org/10.1186/1471-2148-4-44.
Sekiguchi Y, Ohashi A, Parks DH, Yamauchi T, Tyson GW, Hugenholtz P. First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking. PeerJ. 2015;3(1):e740. https://doi.org/10.7717/peerj.740.
Yarza P, Yilmaz P, Pruesse E, et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol. 2014;12(9):635-645. https://doi.org/10.1038/nrmicro3330.
Hug LA, Baker BJ, Anantharaman K, et al. A new view of the tree of life. Nat Microbiol. 2016;1(5):16048. https://doi.org/10.1038/nmicrobiol.2016.48.
Nikolaki S, Tsiamis G. Microbial diversity in the era of omic technologies. Biomed Res Int. 2013;2013:958719-958715. https://doi.org/10.1155/2013/958719.
Hugenholtz P. Exploring prokaryotic diversity in the genomic era. Genome Biol. 2002;3(2):REVIEWS0003. https://doi.org/10.1186/gb-2002-3-2-reviews0003.
Bertani I, Abbruscato P, Piffanelli P, Subramoni S, Venturi V. Rice bacterial endophytes: isolation of a collection, identification of beneficial strains and microbiome analysis. Environ Microbiol Rep. 2016;8(3):388-398. https://doi.org/10.1111/1758-2229.12403.
Kolton M, Sela N, Elad Y, Cytryn E. Comparative genomic analysis indicates that niche adaptation of terrestrial flavobacteria is strongly linked to plant glycan metabolism. PLoS One. 2013;8(9):e76704. https://doi.org/10.1371/journal.pone.0076704.
Hartman K, van der Heijden MGA, Roussely-Provent V, Walser J-C, Schlaeppi K. Deciphering composition and function of the root microbiome of a legume plant. Microbiome. 2017;5(1):2. https://doi.org/10.1186/s40168-016-0220-z.
Björklund AK, Ekman D, Elofsson A. Expansion of protein domain repeats. PLoS Comput Biol. 2006;2(8):e114. https://doi.org/10.1371/journal.pcbi.0020114.
Grishin SY, Deryusheva EI, Machulin AV, et al. Amyloidogenic propensities of ribosomal S1 proteins: bioinformatics screening and experimental checking. Int J Mol Sci. 2020;21(15):5199. https://doi.org/10.3390/ijms21155199.
Agrawal V, Kishan KVR. OB-fold: growing bigger with functional consistency. Curr Protein Pept Sci. 2003;4(3):195-206. https://doi.org/10.2174/1389203033487207.
Sirand-Pugnet P, Lartigue C, Marenda M, et al. Being pathogenic, plastic, and sexual while living with a nearly minimal bacterial genome. PLoS Genet. 2007;3(5):744-758. https://doi.org/10.1371/journal.pgen.0030075.
Amblar M, Barbas A, Gomez-Puertas P, Arraiano CM. The role of the S1 domain in exoribonucleolytic activity: substrate specificity and multimerization. RNA. 2007;13(3):317-327. https://doi.org/10.1261/rna.220407.
Jeffares DC, Tomiczek B, Sojo V, dos Reis M. A beginners guide to estimating the non-synonymous to synonymous rate ratio of all protein-coding genes in a genome. Methods Mol Biol. 2015;1201:65-90. https://doi.org/10.1007/978-1-4939-1438-8_4.
Kosiol C, Vinar T, da Fonseca RR, et al. Patterns of positive selection in six mammalian genomes. PLoS Genet. 2008;4(8):e1000144. https://doi.org/10.1371/journal.pgen.1000144.
Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation. Trends Ecol Evol. 2000;15(12):496-503. https://doi.org/10.1016/S0169-5347(00)01994-7.
Swanson WJ, Yang Z, Wolfner MF, Aquadro CF. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc Natl Acad Sci U S A. 2001;98(5):2509-2514. https://doi.org/10.1073/pnas.051605998.
Anisimova M, Bielawski JP, Yang Z. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol. 2001;18(8):1585-1592. https://doi.org/10.1093/oxfordjournals.molbev.a003945.
Sullivan J, Joyce P. Model selection in phylogenetics. Annu Rev Ecol Evol Syst. 2005;36(1):445-466. https://doi.org/10.1146/annurev.ecolsys.36.102003.152633.
Posada D, Crandall KA. Selecting the best-fit model of nucleotide substitution. Syst Biol. 2001;50(4):580-601. https://doi.org/10.1080/10635150118469.
Bycroft M, Hubbard TJ, Proctor M, Freund SM, Murzin AG. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell. 1997;88(2):235-242. https://doi.org/10.1016/S0092-8674(00)81844-9.
Bhattacharjee N, Biswas P. Position-specific propensities of amino acids in the β-strand. BMC Struct Biol. 2010;10(1):29. https://doi.org/10.1186/1472-6807-10-29.
Richardson JS, Richardson DC. Natural β-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc Natl Acad Sci U S A. 2002;99(5):2754-2759. https://doi.org/10.1073/pnas.052706099.
Andrade MA, Perez-Iratxeta C, Ponting CP. Protein repeats: structures, functions, and evolution. J Struct Biol. 2001;134(2-3):117-131. https://doi.org/10.1006/jsbi.2001.4392.
Ponting CP, Russell RB. Identification of distant homologues of fibroblast growth factors suggests a common ancestor for all beta-trefoil proteins. J Mol Biol. 2000;302(5):1041-1047. https://doi.org/10.1006/jmbi.2000.4087.
Battistuzzi FU, Hedges SB. A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol. 2009;26(2):335-343. https://doi.org/10.1093/molbev/msn247.
Robertson LA, Kuenen JG. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, eds. The Prokaryotes. Vol 5. New York: Springer; 2006. https://doi.org/10.1007/0-387-30745-1.
Williams KP, Kelly DP. Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria. Int J Syst Evol Microbiol. 2013;63(PART 8):2901-2906. https://doi.org/10.1099/ijs.0.049270-0.
Gupta RS. The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev. 2000;24(4):367-402. https://doi.org/10.1111/j.1574-6976.2000.tb00547.x.
Gupta RS, Sneath PHA. Application of the character compatibility approach to generalized molecular sequence data: branching order of the proteobacterial subdivisions. J Mol Evol. 2007;64(1):90-100. https://doi.org/10.1007/s00239-006-0082-2.
Griffiths E, Gupta RS. Signature sequences in diverse proteins provide evidence for the late divergence of the order aquificales. Int Microbiol. 2004;7(1):41-52. https://doi.org/10.2436/im.v7i1.9443.
Boussau B, Guéguen L, Gouy M. Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of aquificales in the phylogeny of bacteria. BMC Evol Biol. 2008;8(1):272. https://doi.org/10.1186/1471-2148-8-272.
Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE. The ecology of acidobacteria: moving beyond genes and genomes. Front Microbiol. 2016;7(MAY):744. https://doi.org/10.3389/fmicb.2016.00744.
Spring S, Schulze R, Overmann J, Schleifer K-H. Identification and characterization of ecologically significant prokaryotes in the sediment of freshwater lakes: molecular and cultivation studies. FEMS Microbiol Rev. 2000;24(5):573-590. https://doi.org/10.1111/j.1574-6976.2000.tb00559.x.
Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol. 2001;67(5):2284-2291. https://doi.org/10.1128/AEM.67.5.2284-2291.2001.
Olson CM, Fikrig E, Anguita J. Host defenses to spirochetes. Clinical Immunology: Principles and Practice. 4th ed. London: Saunders; 2013:338-345. https://doi.org/10.1016/B978-0-7234-3691-1.00016-7.
Kamneva OK, Knight SJ, Liberles DA, Ward NL. Analysis of genome content evolution in pvc bacterial super-phylum: assessment of candidate genes associated with cellular organization and lifestyle. Genome Biol Evol. 2012;4(12):1375-1390. https://doi.org/10.1093/gbe/evs113.
Cho JC, Vergin KL, Morris RM, Giovannoni SJ. Lentisphaera araneosa gen. Nov., sp. nov, a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum, Lentisphaerae. Environ Microbiol. 2004;6(6):611-621. https://doi.org/10.1111/j.1462-2920.2004.00614.x.
Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev. 2013;37(5):634-663. https://doi.org/10.1111/1574-6976.12028.
Thomas F, Hehemann J-H, Rebuffet E, Czjzek M, Michel G. Environmental and gut bacteroidetes: the food connection. Front Microbiol. 2011;2(MAY):93. https://doi.org/10.3389/fmicb.2011.00093.
Shih PM, Hemp J, Ward LM, Matzke NJ, Fischer WW. Crown group oxyphotobacteria postdate the rise of oxygen. Geobiology. 2017;15(1):19-29. https://doi.org/10.1111/gbi.12200.
Xiong J. Molecular evidence for the early evolution of photosynthesis. Science (80- ). 2000;289(5485):1724-1730. https://doi.org/10.1126/science.289.5485.1724.
Blankenship RE. Origin and early evolution of photosynthesis. Photosynth Res. 1992;33(2):91-111. https://doi.org/10.1007/BF00039173.
Lang JM, Darling AE, Eisen JA. Phylogeny of bacterial and archaeal genomes using conserved genes: supertrees and supermatrices. PLoS One. 2013;8(4):e62510. https://doi.org/10.1371/journal.pone.0062510.
Rinke C, Schwientek P, Sczyrba A, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499(7459):431-437. https://doi.org/10.1038/nature12352.
Neimark H. Phylogenetic relationships between mycoplasmas and other prokaryotes. The Mycoplasmas. 1979;1:43-61. https://doi.org/10.1099/00207713-42-2-226.
Bhugra B, Dybvig K. High-frequency rearrangements in the chromosome of mycoplasma pulmonis correlate with phenotypic switching. Mol Microbiol. 1992;6(9):1149-1154. https://doi.org/10.1111/j.1365-2958.1992.tb01553.x.
Borkhsenius SN, Chernova OA, Chernov VM, Vonskii MS. Mycoplasmas [in Russian]. St. Petersburg: Nauka; 2002.
Blanchard A. Ureaplasma urealyticum urease genes; use of a UGA tryptophan codon. Mol Microbiol. 1990;4(4):669-676. https://doi.org/10.1111/j.1365-2958.1990.tb00636.x.
Abadi S, Azouri D, Pupko T, Mayrose I. Model selection may not be a mandatory step for phylogeny reconstruction. Nat Commun. 2019;10(1):934. https://doi.org/10.1038/s41467-019-08822-w.