Phage-encoded ribosomal protein S21 expression is linked to late-stage phage replication

Lin-Xing Chen; Alexander L Jaffe; Adair L Borges; Petar I Penev; Tara Colenbrander Nelson; Lesley A Warren; Jillian F Banfield

doi:10.1038/s43705-022-00111-w

Phage-encoded ribosomal protein S21 expression is linked to late-stage phage replication

ISME Commun. 2022 Mar 30;2(1):31. doi: 10.1038/s43705-022-00111-w.

Authors

Lin-Xing Chen^{1

2}, Alexander L Jaffe³, Adair L Borges², Petar I Penev², Tara Colenbrander Nelson⁴, Lesley A Warren⁴, Jillian F Banfield^{5

6

7

8

9}

Affiliations

¹ Department of Earth and Planetary Science, University of California, Berkeley, CA, USA.
² Innovative Genomics Institute, University of California, Berkeley, CA, USA.
³ Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA.
⁴ Department of Civil and Mineral Engineering, University of Toronto, Toronto, ON, Canada.
⁵ Department of Earth and Planetary Science, University of California, Berkeley, CA, USA. jbanfield@berkeley.edu.
⁶ Innovative Genomics Institute, University of California, Berkeley, CA, USA. jbanfield@berkeley.edu.
⁷ Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA. jbanfield@berkeley.edu.
⁸ Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA, USA. jbanfield@berkeley.edu.
⁹ Chan Zuckerberg Biohub, San Francisco, CA, USA. jbanfield@berkeley.edu.

Abstract

The ribosomal protein S21 (bS21) gene has been detected in diverse viruses with a large range of genome sizes, yet its in situ expression and potential significance have not been investigated. Here, we report five closely related clades of bacteriophages (phages) represented by 47 genomes (8 curated to completion and up to 331 kbp in length) that encode a bS21 gene. The bS21 gene is on the reverse strand within a conserved region that encodes the large terminase, major capsid protein, prohead protease, portal vertex proteins, and some hypothetical proteins. Based on CRISPR spacer targeting, the predominance of bacterial taxonomic affiliations of phage genes with those from Bacteroidetes, and the high sequence similarity of the phage bS21 genes and those from Bacteroidetes classes of Flavobacteriia, Cytophagia and Saprospiria, these phages are predicted to infect diverse Bacteroidetes species that inhabit a range of depths in freshwater lakes. Thus, bS21 phages have the potential to impact microbial community composition and carbon turnover in lake ecosystems. The transcriptionally active bS21-encoding phages were likely in the late stage of replication when collected, as core structural genes and bS21 were highly expressed. Thus, our analyses suggest that the phage bS21, which is involved in translation initiation, substitutes into the Bacteroidetes ribosomes and selects preferentially for phage transcripts during the late-stage replication when large-scale phage protein production is required for assembly of phage particles.