Unlinked rRNA genes are widespread among bacteria and archaea

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Abstract

Ribosomes are essential to cellular life and the genes for their RNA components are the most conserved and transcribed genes in bacteria and archaea. Ribosomal RNA genes are typically organized into a single operon, an arrangement thought to facilitate gene regulation. In reality, some bacteria and archaea do not share this canonical rRNA arrangement—their 16S and 23S rRNA genes are separated across the genome and referred to as “unlinked”. This rearrangement has previously been treated as an anomaly or a byproduct of genome degradation in intracellular bacteria. Here, we leverage complete genome and long-read metagenomic data to show that unlinked 16S and 23S rRNA genes are more common than previously thought. Unlinked rRNA genes occur in many phyla, most significantly within Deinococcus-Thermus, Chloroflexi, and Planctomycetes, and occur in differential frequencies across natural environments. We found that up to 41% of rRNA genes in soil were unlinked, in contrast to the human gut, where all sequenced rRNA genes were linked. The frequency of unlinked rRNA genes may reflect meaningful life history traits, as they tend to be associated with a mix of slow-growing free-living species and intracellular species. We speculate that unlinked rRNA genes may confer selective advantages in some environments, though the specific nature of these advantages remains undetermined and worthy of further investigation. More generally, the prevalence of unlinked rRNA genes in poorly-studied taxa serves as a reminder that paradigms derived from model organisms do not necessarily extend to the broader diversity of bacteria and archaea.

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Data availability

All genomes used in this study were downloaded from NCBI, with assembly IDs listed in Supplementary Dataset S1. All Nanopore data are available at the Sequence Read Archive (SRA) under Bioproject ID PRJNA553237 or the European Nucleotide Archive (ENA) under PRJEB33278. All Moleculo data has been published previously, with publications listed in methods. Classifications and details of both the complete genome and long-read datasets are included in Supplementary Dataset S1 and S2, respectively.

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Acknowledgements

This research was supported in part by the Chateaubriand Fellowship awarded to TEB from the Office for Science & Technology of the Embassy of France in the United States and a grant to NF from the U.S. National Science Foundation (EAR1331828). MA was supported by a research grant (15510) from Villum Fonden. AE gratefully acknowledges the support of a Leverhulme Trust Research Fellowship (RF-2017–652\2). ER was supported by the INCEPTION project (PIA/ANR-16-CONV-0005). We thank Will Trimble for assistance tracking down publicly available Moleculo sequences, Michael Engel for figure design input, and Eric Johnston for early discussions on unlinked rRNA genes.

Author information

TEB, ER, and NF conceived and designed the project and wrote the paper with input from all co-authors. AE, MA, and RK performed the Nanopore sequencing. TEB performed all analyses.

Correspondence to Tess E. Brewer.

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MA and RK own a portion of the company DNASense.

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Brewer, T.E., Albertsen, M., Edwards, A. et al. Unlinked rRNA genes are widespread among bacteria and archaea. ISME J (2019) doi:10.1038/s41396-019-0552-3

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