Alexander A. Radecki, Ariana Fantasia-Davis, Juan S. Maldonado, Joshua W. Mann, Stephanie Sepulveda-Camacho, Pearl Morosky, Jordan Douglas, Oscar Vargas-Rodriguez
{"title":"与大肠杆菌共存的细菌氨基酰-tRNA 合成酶同系物表现出不同的系统发育背景和功能兼容性。","authors":"Alexander A. Radecki, Ariana Fantasia-Davis, Juan S. Maldonado, Joshua W. Mann, Stephanie Sepulveda-Camacho, Pearl Morosky, Jordan Douglas, Oscar Vargas-Rodriguez","doi":"10.1002/iub.2920","DOIUrl":null,"url":null,"abstract":"<p>Aminoacyl-tRNA synthetases (aaRSs) are universally essential enzymes that synthesize aminoacyl-tRNA substrates for protein synthesis. Although most organisms require a single aaRS gene for each proteinogenic amino acid to translate their genetic information, numerous species encode multiple gene copies of an aaRS. Growing evidence indicates that organisms acquire extra aaRS genes to sustain or adapt to their unique lifestyle. However, predicting and defining the function of repeated aaRS genes remains challenging due to their potentially unique physiological role in the host organism and the inconsistent annotation of repeated aaRS genes in the literature. Here, we carried out comparative, phylogenetic, and functional studies to determine the activity of coexisting paralogs of tryptophanyl-, tyrosyl-, seryl-, and prolyl-tRNA synthetases encoded in several human pathogenic bacteria. Our analyses revealed that, with a few exceptions, repeated aaRSs involve paralogous genes with distinct phylogenetic backgrounds. Using a collection of <i>Escherichia coli</i> strains that enabled the facile characterization of aaRS activity in vivo, we found that, in almost all cases, one aaRS displayed transfer RNA (tRNA) aminoacylation activity, whereas the other was not compatible with <i>E</i>. <i>coli</i>. Together, this work illustrates the challenges of identifying, classifying, and predicting the function of aaRS paralogs and highlights the complexity of aaRS evolution. Moreover, these results provide new insights into the potential role of aaRS paralogs in the biology of several human pathogens and foundational knowledge for the investigation of the physiological role of repeated aaRS paralogs across bacteria.</p>","PeriodicalId":14728,"journal":{"name":"IUBMB Life","volume":"76 12","pages":"1139-1153"},"PeriodicalIF":3.7000,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Coexisting bacterial aminoacyl-tRNA synthetase paralogs exhibit distinct phylogenetic backgrounds and functional compatibility with Escherichia coli\",\"authors\":\"Alexander A. Radecki, Ariana Fantasia-Davis, Juan S. Maldonado, Joshua W. Mann, Stephanie Sepulveda-Camacho, Pearl Morosky, Jordan Douglas, Oscar Vargas-Rodriguez\",\"doi\":\"10.1002/iub.2920\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Aminoacyl-tRNA synthetases (aaRSs) are universally essential enzymes that synthesize aminoacyl-tRNA substrates for protein synthesis. Although most organisms require a single aaRS gene for each proteinogenic amino acid to translate their genetic information, numerous species encode multiple gene copies of an aaRS. Growing evidence indicates that organisms acquire extra aaRS genes to sustain or adapt to their unique lifestyle. However, predicting and defining the function of repeated aaRS genes remains challenging due to their potentially unique physiological role in the host organism and the inconsistent annotation of repeated aaRS genes in the literature. Here, we carried out comparative, phylogenetic, and functional studies to determine the activity of coexisting paralogs of tryptophanyl-, tyrosyl-, seryl-, and prolyl-tRNA synthetases encoded in several human pathogenic bacteria. Our analyses revealed that, with a few exceptions, repeated aaRSs involve paralogous genes with distinct phylogenetic backgrounds. Using a collection of <i>Escherichia coli</i> strains that enabled the facile characterization of aaRS activity in vivo, we found that, in almost all cases, one aaRS displayed transfer RNA (tRNA) aminoacylation activity, whereas the other was not compatible with <i>E</i>. <i>coli</i>. Together, this work illustrates the challenges of identifying, classifying, and predicting the function of aaRS paralogs and highlights the complexity of aaRS evolution. Moreover, these results provide new insights into the potential role of aaRS paralogs in the biology of several human pathogens and foundational knowledge for the investigation of the physiological role of repeated aaRS paralogs across bacteria.</p>\",\"PeriodicalId\":14728,\"journal\":{\"name\":\"IUBMB Life\",\"volume\":\"76 12\",\"pages\":\"1139-1153\"},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2024-10-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"IUBMB Life\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1002/iub.2920\",\"RegionNum\":3,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"IUBMB Life","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/iub.2920","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
Coexisting bacterial aminoacyl-tRNA synthetase paralogs exhibit distinct phylogenetic backgrounds and functional compatibility with Escherichia coli
Aminoacyl-tRNA synthetases (aaRSs) are universally essential enzymes that synthesize aminoacyl-tRNA substrates for protein synthesis. Although most organisms require a single aaRS gene for each proteinogenic amino acid to translate their genetic information, numerous species encode multiple gene copies of an aaRS. Growing evidence indicates that organisms acquire extra aaRS genes to sustain or adapt to their unique lifestyle. However, predicting and defining the function of repeated aaRS genes remains challenging due to their potentially unique physiological role in the host organism and the inconsistent annotation of repeated aaRS genes in the literature. Here, we carried out comparative, phylogenetic, and functional studies to determine the activity of coexisting paralogs of tryptophanyl-, tyrosyl-, seryl-, and prolyl-tRNA synthetases encoded in several human pathogenic bacteria. Our analyses revealed that, with a few exceptions, repeated aaRSs involve paralogous genes with distinct phylogenetic backgrounds. Using a collection of Escherichia coli strains that enabled the facile characterization of aaRS activity in vivo, we found that, in almost all cases, one aaRS displayed transfer RNA (tRNA) aminoacylation activity, whereas the other was not compatible with E. coli. Together, this work illustrates the challenges of identifying, classifying, and predicting the function of aaRS paralogs and highlights the complexity of aaRS evolution. Moreover, these results provide new insights into the potential role of aaRS paralogs in the biology of several human pathogens and foundational knowledge for the investigation of the physiological role of repeated aaRS paralogs across bacteria.
期刊介绍:
IUBMB Life is the flagship journal of the International Union of Biochemistry and Molecular Biology and is devoted to the rapid publication of the most novel and significant original research articles, reviews, and hypotheses in the broadly defined fields of biochemistry, molecular biology, cell biology, and molecular medicine.