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Intragenic DNA inversions expand bacterial coding capacity

  • van der Woude, M. W. & Bäumler, A. J. Phase and antigenic variation in bacteria. Clin. Microbiol. Rev. 17, 581–611 (2004).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Trzilova, D. & Tamayo, R. Site-specific recombination—how simple DNA inversions produce complex phenotypic heterogeneity in bacterial populations. Trends Genet. 37, 59–72 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zieg, J., Silverman, M., Hilmen, M. & Simon, M. Recombinational switch for gene expression. Science 196, 170–172 (1977).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Stocker, B. A. Measurements of rate of mutation of flagellar antigenic phase in Salmonella typhimurium. J. Hyg. 47, 398–413 (1949).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meydan, S., Vázquez-Laslop, N. & Mankin, A. S. Genes within genes in bacterial genomes. Microbiol. Spectr. 6, rwr-0020-2018 (2018).

    Article 

    Google Scholar
     

  • Zhong, A. et al. Toxic antiphage defense proteins inhibited by intragenic antitoxin proteins. Proc. Natl Acad. Sci. USA 120, e2307382120 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Moxon, R., Bayliss, C. & Hood, D. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet. 40, 307–333 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sberro, H. et al. Large-scale analyses of human microbiomes reveal thousands of small, novel genes. Cell 178, 1245–1259.e14 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schlub, T. E. & Holmes, E. C. Properties and abundance of overlapping genes in viruses. Virus Evol. 6, veaa009 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Medhekar, B. & Miller, J. F. Diversity-generating retroelements. Curr. Opin. Microbiol. 10, 388–395 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Andrewes, F. W. Studies in group-agglutination I. The Salmonella group and its antigenic structure. J. Pathol. Bacteriol. 25, 505–521 (1922).

    Article 

    Google Scholar
     

  • Goldberg, A., Fridman, O., Ronin, I. & Balaban, N. Q. Systematic identification and quantification of phase variation in commensal and pathogenic Escherichia coli. Genome Med. 6, 112 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sekulovic, O. et al. Genome-wide detection of conservative site-specific recombination in bacteria. PLoS Genet. 14, e1007332 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jiang, X. et al. Invertible promoters mediate bacterial phase variation, antibiotic resistance, and host adaptation in the gut. Science 363, 181–187 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Milman, O., Yelin, I. & Kishony, R. Systematic identification of gene-altering programmed inversions across the bacterial domain. Nucleic Acids Res. 51, 553–573 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Komano, T. Shufflons: multiple inversion systems and integrons. Annu. Rev. Genet. 33, 171–191 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Atack, J. M., Guo, C., Yang, L., Zhou, Y. & Jennings, M. P. DNA sequence repeats identify numerous type I restriction-modification systems that are potential epigenetic regulators controlling phase-variable regulons; phasevarions. FASEB J. 34, 1038–1051 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chatzidaki-Livanis, M., Coyne, M. J., Roche-Hakansson, H. & Comstock, L. E. Expression of a uniquely regulated extracellular polysaccharide confers a large-capsule phenotype to Bacteroides fragilis. J. Bacteriol. 190, 1020–1026 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Taketani, M., Donia, M. S., Jacobson, A. N., Lambris, J. D. & Fischbach, M. A. A phase-variable surface layer from the gut symbiont Bacteroides thetaiotaomicron. mBio 6, e01339-15 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Troy, E. B., Carey, V. J., Kasper, D. L. & Comstock, L. E. Orientations of the Bacteroides fragilis capsular polysaccharide biosynthesis locus promoters during symbiosis and infection. J. Bacteriol. 192, 5832–5836 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Severyn, C. J. et al. Microbiota dynamics in a randomized trial of gut decontamination during allogeneic hematopoietic cell transplantation. JCI Insight 7, e154344 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Siranosian, B. A. et al. Rare transmission of commensal and pathogenic bacteria in the gut microbiome of hospitalized adults. Nat. Commun. 13, 586 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Martens, E. C., Chiang, H. C. & Gordon, J. I. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447–457 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Martens, E. C., Roth, R., Heuser, J. E. & Gordon, J. I. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J. Biol. Chem. 284, 18445–18457 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krinos, C. M. et al. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414, 555–558 (2001).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Porter, N. T. et al. Phase-variable capsular polysaccharides and lipoproteins modify bacteriophage susceptibility in Bacteroides thetaiotaomicron. Nat. Microbiol. 5, 1170–1181 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Round, J. L. et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974–977 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Neff, C. P. et al. Diverse intestinal bacteria contain putative zwitterionic capsular polysaccharides with anti-inflammatory properties. Cell Host Microbe 20, 535–547 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mazmanian, S. K., Liu, C. H., Tzianabos, A. O. & Kasper, D. L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107–118 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Porter, N. T., Canales, P., Peterson, D. A. & Martens, E. C. A Subset of polysaccharide capsules in the human symbiont Bacteroides thetaiotaomicron promote increased competitive fitness in the mouse gut. Cell Host Microbe 22, 494–506.e8 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Musumeci, O. et al. Intragenic inversion of mtDNA: a new type of pathogenic mutation in a patient with mitochondrial myopathy. Am. J. Hum. Genet. 66, 1900–1904 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Smyshlyaev, G., Bateman, A. & Barabas, O. Sequence analysis of tyrosine recombinases allows annotation of mobile genetic elements in prokaryotic genomes. Mol. Syst. Biol. 17, e9880 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • West, P. T., Chanin, R. B. & Bhatt, A. S. From genome structure to function: insights into structural variation in microbiology. Curr. Opin. Microbiol. 69, 102192 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • van Kempen, M. et al. Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. 42, 243–246 (2024).

    Article 
    PubMed 

    Google Scholar
     

  • Casino, P., Rubio, V. & Marina, A. The mechanism of signal transduction by two-component systems. Curr. Opin. Struct. Biol. 20, 763–771 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Loenen, W. A. M., Dryden, D. T. F., Raleigh, E. A. & Wilson, G. G. Type I restriction enzymes and their relatives. Nucleic Acids Res. 42, 20–44 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • De Ste Croix, M. et al. Phase-variable methylation and epigenetic regulation by type I restriction-modification systems. FEMS Microbiol. Rev. 41, S3–S15 (2017).

    Article 

    Google Scholar
     

  • Chen, L. et al. Short- and long-read metagenomics expand individualized structural variations in gut microbiomes. Nat. Commun. 13, 3175 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maghini, D. G. et al. Quantifying bias introduced by sample collection in relative and absolute microbiome measurements. Nat. Biotechnol. 42, 328–338 (2024).

  • Rodionov, D. A. et al. Micronutrient requirements and sharing capabilities of the human gut microbiome. Front. Microbiol. 10, 1316 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sharma, V. et al. B-vitamin sharing promotes stability of gut microbial communities. Front. Microbiol. 10, 1485 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Costliow, Z. A. & Degnan, P. H. Thiamine acquisition strategies impact metabolism and competition in the gut microbe Bacteroides thetaiotaomicron. mSystems 2, e00116–17 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Martinez-Gomez, N. C. & Downs, D. M. ThiC is an [Fe-S] cluster protein that requires AdoMet to generate the 4-amino-5-hydroxymethyl-2-methylpyrimidine moiety in thiamin synthesis. Biochemistry 47, 9054–9056 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Said, H. M. Intestinal absorption of water-soluble vitamins in health and disease. Biochem. J. 437, 357–372 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • D’Souza, G. et al. Less is more: selective advantages can explain the prevalent loss of biosynthetic genes in bacteria. Evolution 68, 2559–2570 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Jurgenson, C. T., Ealick, S. E. & Begley, T. P. Biosynthesis of thiamin pyrophosphate. EcoSal Plus https://doi.org/10.1128/ecosalplus.3.6.3.7 (2009).

  • Rodionov, D. A., Vitreschak, A. G., Mironov, A. A. & Gelfand, M. S. Comparative genomics of thiamin biosynthesis in prokaryotes. J. Biol. Chem. 277, 48949–48959 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bacic, M. K. & Smith, C. J. Laboratory maintenance and cultivation of bacteroides species. Curr. Protoc. Microbiol. https://doi.org/10.1002/9780471729259.mc13c01s9 (2008).

  • Zhu, W. et al. Xenosiderophore utilization promotes Bacteroides thetaiotaomicron resilience during colitis. Cell Host Microbe 27, 376–388.e8 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).

  • Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang, C., Chu, J., Warren, R. L. & Birol, I. NanoSim: nanopore sequence read simulator based on statistical characterization. Gigascience 6, gix010 (2017).

    Article 

    Google Scholar
     

  • Ono, Y., Asai, K. & Hamada, M. PBSIM2: a simulator for long-read sequencers with a novel generative model of quality scores. Bioinformatics 37, 589–595 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • De Coster, W., D’Hert, S., Schultz, D. T., Cruts, M. & Van Broeckhoven, C. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics 34, 2666–2669 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meng, E. C. et al. UCSF ChimeraX: tools for structure building and analysis. Protein Sci. 32, e4792 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aramaki, T. et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 36, 2251–2252 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article 
    ADS 
    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paysan-Lafosse, T. et al. InterPro in 2022. Nucleic Acids Res. 51, D418–D427 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289–300 (1995).

    Article 
    MathSciNet 

    Google Scholar
     

  • Prjibelski, A., Antipov, D., Meleshko, D., Lapidus, A. & Korobeynikov, A. Using SPAdes de novo assembler. Curr. Protoc. Bioinformatics 70, e102 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lin, Y. et al. Assembly of long error-prone reads using de Bruijn graphs. Proc. Natl Acad. Sci. USA 113, E8396–E8405 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Skowronek, P. et al. Rapid and in-depth coverage of the (phospho-)proteome with deep libraries and optimal window design for dia-PASEF. Mol. Cell. Proteomics 21, 100279 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kong, A. T., Leprevost, F. V., Avtonomov, D. M., Mellacheruvu, D. & Nesvizhskii, A. I. MSFragger: ultrafast and comprehensive peptide identification in mass spectrometry-based proteomics. Nat. Methods 14, 513–520 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Demichev, V., Messner, C. B., Vernardis, S. I., Lilley, K. S. & Ralser, M. DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput. Nat. Methods 17, 41–44 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966–968 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pino, L. K. et al. The Skyline ecosystem: informatics for quantitative mass spectrometry proteomics. Mass Spectrom. Rev. 39, 229–244 (2020).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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