Occurrence of randomly recombined functional 16S rRNA genes in Thermus thermophilus suggests genetic interoperability and promiscuity of bacterial 16S rRNAs

Based on the structural complexity of ribosomes, 16S rRNA genes are considered species-specific and hence used for bacterial phylogenetic analysis. However, a growing number of reports suggest the occurrence of horizontal gene transfer, raising genealogical questions. Here we show the genetic interoperability and promiscuity of 16S rRNA in the ribosomes of an extremely thermophilic bacterium, Thermus thermophilus. The gene in this thermophile was systematically replaced with a diverse array of heterologous genes, resulting in the discovery of various genes that supported growth, some of which were from different phyla. Moreover, numerous functional chimeras were spontaneously generated. Remarkably, cold-adapted mutants were obtained carrying chimeric or full-length heterologous genes, indicating that horizontal gene transfer promoted adaptive evolution. The ribosome may well be understood as a patchworked supramolecule comprising patchworked components. We here propose the “random patch model” for ribosomal evolution.

• Publication year

  2019

• Venue

  Scientific Reports

• Publication date

  2019-08-02

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/s41598-019-47807-zPMID 31375780PMCID 6677816
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Phylogenetic Networks

  2019cited by this paper
• Temperature-dependent expression of different guanine-plus-cytosine content 16S rRNA genes in Haloarcula strains of the class Halobacteria

  2018cited by this paper
• PCR Primer Design for 16S rRNAs for Experimental Horizontal Gene Transfer Test in Escherichia coli

  2017cited by this paper
• Comparative RNA function analysis reveals high functional similarity between distantly related bacterial 16 S rRNAs

  2017cited by this paper
• Phylogenetic Network Analysis Revealed the Occurrence of Horizontal Gene Transfer of 16S rRNA in the Genus Enterobacter

  2017cited by this paper
• History of the ribosome and the origin of translation

  2015cited by this paper
• Intragenomic Heterogeneity of 16S rRNA Genes Causes Overestimation of Prokaryotic Diversity

  2013cited by this paper
• The Variability of the 16S rRNA Gene in Bacterial Genomes and Its Consequences for Bacterial Community Analyses

  2013cited by this paper
• Revisiting bacterial phylogeny

  2013cited by this paper
• Reconstitution of translation from Thermus thermophilus reveals a minimal set of components sufficient for protein synthesis at high temperatures and functional conservation of modern and ancient translation components

  2012cited by this paper
• Mutational robustness of 16S ribosomal RNA, shown by experimental horizontal gene transfer in Escherichia coli

  2012cited by this paper
• Promiscuous behaviour of archaeal ribosomal proteins: Implications for eukaryotic ribosome evolution

  2012cited by this paper
• Systematic chromosomal deletion of bacterial ribosomal protein genes.

  2011cited by this paper
• Recruitment of a species-specific translational arrest module to monitor different cellular processes

  2011cited by this paper
• An Extreme Thermophile, Thermus thermophilus, Is a Polyploid Bacterium

  2010cited by this paper
• Origin and evolution of the ribosome.

  2010cited by this paper
• Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4

  2009cited by this paper
• Peeling the onion: ribosomes are ancient molecular fossils.

  2009cited by this paper
• Molecular signatures of ribosomal evolution

  2008cited by this paper
• The origin and evolution of the ribosome

  2008cited by this paper
• Database indexing for production MegaBLAST searches

  2008cited by this paper
• Thermal Adaptation of the Small Subunit Ribosomal RNA Gene: A Comparative Study

  2006cited by this paper
• Deleterious mutations in small subunit ribosomal RNA identify functional sites and potential targets for antibiotics.

  2005cited by this paper
• Compensatory neutral mutations and the evolution of RNA

  2004cited by this paper
• The genome sequence of the extreme thermophile Thermus thermophilus

  2004cited by this paper
• Phylogenetic networks

  2004cited by this paper
• Protein building blocks preserved by recombination

  2002cited by this paper
• On the evolution of cells

  2002cited by this paper
• Simultaneous Horizontal Gene Transfer of a Gene Coding for Ribosomal Protein L27 and Operational Genes in Arthrobacter Sp.

  2002cited by this paper
• Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins

  2001cited by this paper
• Structure of the 30S ribosomal subunit

  2000cited by this paper
• The evolutionary history of ribosomal protein RpS14: horizontal gene transfer at the heart of the ribosome.

  2000cited by this paper
• Interpreting the universal phylogenetic tree.

  2000cited by this paper
• A Greedy Algorithm for Aligning DNA Sequences

  2000cited by this paper
• Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima

  1999cited by this paper
• Horizontal gene transfer among genomes: the complexity hypothesis.

  1999cited by this paper
• Functional implications of ribosomal protein L2 in protein biosynthesis as shown by in vivo replacement studies.

  1998cited by this paper
• The complete genome of the hyperthermophilic bacterium Aquifex aeolicus

  1998cited by this paper
• Compensatory neutral mutations and the evolution of RNA.

  1998cited by this paper
• Different consequences of incorporating chloroplast ribosomal proteins L12 and S18 into the bacterial ribosomes of Escherichia coli.

  1997cited by this paper
• Pyrimidine biosynthesis genes (pyrE and pyrF) of an extreme thermophile, Thermus thermophilus

  1996cited by this paper
• The Taxonomy and Identification of Thermus

  1995cited by this paper
• Thermus thermophilus 16S rRNA is transcribed from an isolated transcription unit

  1989cited by this paper
• Bacterial evolution

  1987cited by this paper
• Genetic transformation of the extreme thermophile Thermus thermophilus and of other Thermus spp

  1986cited by this paper
• Description of Thermus thermophilus (Yoshida and Oshima) comb. nov., a Nonsporulating Thermophilic Bacterium from a Japanese Thermal Spa

  1974cited by this paper

• Development of new Thermus thermophilus—Escherichia coli shuttle vectors

  2025cites this paper
• SyFi: generating and using sequence fingerprints to distinguish SynCom isolates

  2025cites this paper
• The overlooked evolutionary dynamics of 16S rRNA revises its role as the “gold standard” for bacterial species identification

  2024cites this paper
• Complete genome sequences of Thermus thermophilus strains isolated from Shirahama Hot Spring in Japan

  2024cites this paper
• Comparison of the full-length sequence and sub-regions of 16S rRNA gene for skin microbiome profiling

  2024cites this paper
• Microbial adaptation to different environmental conditions: molecular perspective of evolved genetic and cellular systems

  2022cites this paper
• Phylogenetic trees of closely related bacterial species and subspecies based on frequencies of short nucleotide sequences

  2022cites this paper
• Complete Genome Sequences of Thermus Strains Isolated from Senami Hot Spring in Japan

  2022cites this paper
• The 16S rRNA Gene Is Not a Precise Classifier for Luteibacter Species

  2022cites this paper
• Throughput screening of Bacillus subtilis strains that abundantly secrete surfactin in vitro identifies effective probiotic candidates

  2022cites this paper
• Complete Genome Sequence of Thermus thermophilus Strain HB5018, Isolated from Mine Hot Spring in Japan

  2021cites this paper
• Complete Genome Sequences of Thermus thermophilus Strains HB5002 and HB5008, Isolated from Mine Hot Spring in Japan

  2021cites this paper
• Evidence of Horizontal Gene Transfer of 50S Ribosomal Genes rplB, rplD, and rplY in Neisseria gonorrhoeae

  2021cites this paper
• Microbiome–Gut Dissociation: Investigating the Origins of Obesity

  2021cites this paper
• Complete Genome Resequencing of Thermus thermophilus Strain TMY by Hybrid Assembly of Long- and Short-Read Sequencing Technologies

  2021cites this paper
• Prospective nucleotide sequence analysis of methicillin resistant Staphylococcus aureus isolates from Sokoto state

  2020cites this paper
• Complete Genome Sequences of Rhodothermus marinus Strains AA2-13 and AA3-38, Isolated from Arima Onsen Hot Spring in Japan

  2020cites this paper
• Recent advances in understanding extremophiles

  2019cites this paper
• Taxonomic resolution of the ribosomal RNA operon in bacteria: implications for its use with long-read sequencing

  2019cites this paper