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Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage–host interactions

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Abstract

The 104 kb genome of cold-active bacteriophage 9A, which replicates in the marine psychrophilic gamma-proteobacterium Colwellia psychrerythraea strain 34H (between −12 and 8 °C), was sequenced and analyzed to investigate elements of molecular adaptation to low temperature and phage–host interactions in the cold. Most characterized ORFs indicated closest similarity to gamma-proteobacteria and their phages, though no single module provided definitive phylogenetic grouping. A subset of primary structural features linked to psychrophily suggested that the majority of annotated phage proteins were not psychrophilic; those that were, primarily serve phage-specific functions and may also contribute to 9A’s restricted temperature range for replication as compared to host. Comparative analyses suggest ribonucleotide reductase genes were acquired laterally from host. Neither restriction modification nor the CRISPR-Cas system appeared to be the predominant phage defense mechanism of Cp34H or other cold-adapted bacteria; we hypothesize that psychrophilic hosts rely more on the use of extracellular polymeric material to block cell surface receptors recognized by phages. The relative dearth of evidence for genome-specific defenses, genetic transfer events or auxiliary metabolic genes suggest that the 9A-Cp34H system may be less tightly coupled than are other genomically characterized marine phage–host systems, with possible implications for phage specificity under different environmental conditions.

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Abbreviations

9A:

Colwelliaphage 9A

11b:

Flavobacteriophage 11b

AMG:

Auxiliary metabolic gene

CDS:

Coding sequence corresponding to sequence of amino acids in predicted protein including start and stop codons

ch :

Conserved hypothetical protein

Cp34H:

Colwellia psychrerythraea strain 34H

CRISPR:

Clustered regularly interspaced short palindromic repeat

EPS:

Extracellular polymeric substances

LGT:

Lateral gene transfer

MPSP:

Marine Phage Sequencing Project

MT :

Methyltransferase

nr:

NCBI Genbank non-redundant database

nrd:

Ribonucleotide reductase

ORF:

Open reading frame

ORFan:

ORF with no known homolog

PHS:

Phage–host system

pp :

Predicted protein

RE:

Restriction enzyme

RM:

Restriction-modification system

SD:

Standard deviation

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Acknowledgments

Support for this research was provided by NSF IGERT award 0504219, NSF OPP-ANS award 0908724 (JWD), and the Walters Endowed Professorship (JWD). Financial support for genome sequencing was provided by the Betty and Gordon Moore Foundation and performed by the Broad Institute of MIT and Harvard. We appreciate the input of John Baross, William Brazelton, Eric Collins, Gabrielle Rocap, Llyd Wells, members of the UW Center for Environmental Genomics, and anonymous reviewers.

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  1. School of Oceanography and Astrobiology Program, University of Washington, Box 355351, Seattle, WA, 98195, USA

    Jesse R. Colangelo-Lillis & Jody W. Deming

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  1. Jesse R. Colangelo-Lillis
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Correspondence to Jesse R. Colangelo-Lillis.

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Communicated by A. Driessen.

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792_2012_497_MOESM1_ESM.pdf

Fig. S1. Colwelliaphage 9A ORF protein characters compared to mean character value for all 9A ORFs. Each subfigure shows deviation from 9A genome character mean as fraction of that mean for each ORF. Modules separated with vertical lines. * indicates ORF contained no Glutamic Acid (E) residues, but was graphed as though it contained 1. Only ORFs with a minimum of two protein characters values scored as psychrophilic, or one character scored as strongly psychrophilic are shown. Note varying scale of x-axes. See text for definition of character values binned as psychrophilic and strongly psychrophilic and Table S1 for gene abbreviations (PDF 297 kb)

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Table S2 (PDF 133 kb)

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Colangelo-Lillis, J.R., Deming, J.W. Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage–host interactions. Extremophiles 17, 99–114 (2013). https://doi.org/10.1007/s00792-012-0497-1

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