Viruses Infecting a Freshwater Filamentous Cyanobacterium (Nostoc sp.) Encode a Functional CRISPR Array and a Proteobacterial DNA Polymerase B.

Caroline Chénard,Jennifer F Wirth,Curtis A Suttle,Roger Hendrix

doi:10.1128/mbio.00667-16

Abstract

ABSTRACT Here we present the first genomic characterization of viruses infecting Nostoc, a genus of ecologically important cyanobacteria that are widespread in freshwater. Cyanophages A-1 and N-1 were isolated in the 1970s and infect Nostoc sp. strain PCC 7210 but remained genomically uncharacterized. Their 68,304- and 64,960-bp genomes are strikingly different from those of other sequenced cyanophages. Many putative genes that code for proteins with known functions are similar to those found in filamentous cyanobacteria, showing a long evolutionary history in their host. Cyanophage N-1 encodes a CRISPR array that is transcribed during infection and is similar to the DR5 family of CRISPRs commonly found in cyanobacteria. The presence of a host-related CRISPR array in a cyanophage suggests that the phage can transfer the CRISPR among related cyanobacteria and thereby provide resistance to infection with competing phages. Both viruses also encode a distinct DNA polymerase B that is closely related to those found in plasmids of Cyanothece sp. strain PCC 7424, Nostoc sp. strain PCC 7120, and Anabaena variabilis ATCC 29413. These polymerases form a distinct evolutionary group that is more closely related to DNA polymerases of proteobacteria than to those of other viruses. This suggests that the polymerase was acquired from a proteobacterium by an ancestral virus and transferred to the cyanobacterial plasmid. Many other open reading frames are similar to a prophage-like element in the genome of Nostoc sp. strain PCC 7524. The Nostoc cyanophages reveal a history of gene transfers between filamentous cyanobacteria and their viruses that have helped to forge the evolutionary trajectory of this previously unrecognized group of phages.

Highlights

Filamentous cyanobacteria of the genera Nostoc and Anabaena are abundant and active members of aquatic and terrestrial microbial communities
Cyanophage N-1 has a clustered regularly interspaced short palindromic repeats (CRISPRs) array that is similar to those found in cyanobacteria, suggesting that cyanophages play a role in exchanging CRISPRs among cyanobacteria
Cyanophage N-1 contains a CRISPR array similar to those found in cyanobacteria, suggesting that phages may mediate the exchange of CRISPRS among cyanobacteria and confer resistance to competing phages

Summary

Introduction

Filamentous cyanobacteria of the genera Nostoc and Anabaena are abundant and active members of aquatic and terrestrial microbial communities They occur in habitats ranging from the bottom of ice-covered polar lakes [1] and hypertrophic coastal lagoons [2] to rice paddy soils [3] and rock pool communities in karst regions [4]. Despite the ecological importance of these cyanobacteria, the genomic composition of the viruses infecting them remains largely unexplored Bacteria and their viruses (phages) have a shared evolutionary history stretching for billions of years that has led to a myriad of adaptations for cells to avoid infection and countermeasures for phage to escape these defenses [5]. Cyanophage N-1 has a CRISPR array that is similar to those found in cyanobacteria, suggesting that cyanophages play a role in exchanging CRISPRs among cyanobacteria

Methods

Results

Conclusion