Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences.

Simon Roux,François Enault,Didier Debroas,Patrick Forterre,Mart Krupovic

doi:10.1098/rsob.130160

Abstract

Although the importance of viruses in natural ecosystems is widely acknowledged, the functional potential of viral communities is yet to be determined. Viral genomes are traditionally believed to carry only those genes that are directly pertinent to the viral life cycle, though this view was challenged by the discovery of metabolism genes in several phage genomes. Metagenomic approaches extended these analyses to a community scale, and several studies concluded that microbial and viral communities encompass similar functional potentials. However, these conclusions could originate from the presence of cellular DNA within viral metagenomes. We developed a computational method to estimate the proportion and origin of cellular sequences in a set of 67 published viromes. A quarter of the datasets were found to contain a substantial amount of sequences originating from cellular genomes. When considering only viromes with no cellular DNA detected, the functional potential of viral and microbial communities was found to be fundamentally different—a conclusion more consistent with the actual picture drawn from known viruses. Yet a significant number of cellular metabolism genes was still retrieved in these viromes, suggesting that the presence of auxiliary genes involved in various metabolic pathways within viral genomes is a general trend in the virosphere.

Highlights

Studies on the quantitative and functional importance of viruses in natural environments emerged more than 20 years ago with reports on the high concentration of bacteriophages in natural waters [1]
The detection of typical prokaryotic genes never retrieved in a viral genome, such as those coding for ribosomal RNA, indicates that a virome most probably contains DNA from cellular origin
— viromes with a Ribosomal DNA (rDNA) ratio higher than 0.2‰, similar in average to the rDNA ratios observed in microbiomes that can be considered as containing a non-negligible proportion of cellular sequences

Summary

Introduction

Studies on the quantitative and functional importance of viruses in natural environments emerged more than 20 years ago with reports on the high concentration of bacteriophages in natural waters [1]. License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited. Besides the bona fide viral genes (i.e. for virion structure and assembly, and genome replication), several viruses were found to contain ‘auxiliary metabolism genes’. Phosphate metabolism-associated genes, for example, were described in Roseobacter phage SIOI [7], while several photosystem genes were discovered in cyanophages [8,9]. The discovery of such metabolism genes in several viral genomes was one of the elements fuelling the recently renewed debate about the true nature of viruses and their place among cellular life forms [10,11]. The precise range of metabolism-associated genes encompassed in viral genomes is still to be characterized

Methods

Results

Conclusion