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Nitrogen Flow in Diazotrophic Cyanobacterium Aphanizomenon flos-aquae Is Altered by Cyanophage Infection.

ABSTRACT: Viruses can significantly influence cyanobacteria population dynamics and activity, and through this the biogeochemical cycling of major nutrients. However, surprisingly little attention has been given to understand how viral infections alter the ability of diazotrophic cyanobacteria for atmospheric nitrogen fixation and its release to the environment. This study addressed the importance of cyanophages for net 15N2 assimilation rate, expression of nitrogenase reductase gene (nifH) and changes in nitrogen enrichment (15N/14N) in the diazotrophic cyanobacterium Aphanizomenon flos-aquae during infection by the cyanophage vB_AphaS-CL131. We found that while the growth of A. flos-aquae was inhibited by cyanophage addition (decreased from 0.02 h-1 to 0.002 h-1), there were no significant differences in nitrogen fixation rates (control: 22.7 × 10-7 nmol N heterocyte-1; infected: 23.9 × 10-7 nmol N heterocyte-1) and nifH expression level (control: 0.6-1.6 transcripts heterocyte-1; infected: 0.7-1.1 transcripts heterocyte-1) between the infected and control A. flos-aquae cultures. This implies that cyanophage genome replication and progeny production within the vegetative cells does not interfere with the N2 fixation reactions in the heterocytes of these cyanobacteria. However, higher 15N enrichment at the poles of heterocytes of the infected A. flos-aquae, revealed by NanoSIMS analysis indicates the accumulation of fixed nitrogen in response to cyanophage addition. This suggests reduced nitrogen transport to vegetative cells and the alterations in the flow of fixed nitrogen within the filaments. In addition, we found that cyanophage lysis resulted in a substantial release of ammonium into culture medium. Cyanophage infection seems to substantially redirect N flow from cyanobacterial biomass to the production of N storage compounds and N release.

SUBMITTER: Kuznecova J

PROVIDER: S-EPMC7466765 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Nitrogen Flow in Diazotrophic Cyanobacterium Aphanizomenon flos-aquae Is Altered by Cyanophage Infection.

Kuznecova Jolita J Šulčius Sigitas S Vogts Angela A Voss Maren M Jürgens Klaus K Šimoliūnas Eugenijus E

Frontiers in microbiology 20200819

Viruses can significantly influence cyanobacteria population dynamics and activity, and through this the biogeochemical cycling of major nutrients. However, surprisingly little attention has been given to understand how viral infections alter the ability of diazotrophic cyanobacteria for atmospheric nitrogen fixation and its release to the environment. This study addressed the importance of cyanophages for net 15N2 assimilation rate, expression of nitrogenase reductase gene ...[more]

PMID: 32973727

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Project description:While filamentous cyanobacteria play a crucial role in food web dynamics and biogeochemical cycling of many aquatic ecosystems around the globe, the knowledge regarding the phages infecting them is limited. Here, we describe the complete genome of the virulent cyanophage vB_AphaS-CL131 (here, CL 131), a Siphoviridae phage that infects the filamentous diazotrophic bloom-forming cyanobacterium Aphanizomenon flos-aquae in the brackish Baltic Sea. CL 131 features a 112,793-bp double-stranded DNA (dsDNA) genome encompassing 149 putative open reading frames (ORFs), of which the majority (86%) lack sequence homology to genes with known functions in other bacteriophages or bacteria. Phylogenetic analysis revealed that CL 131 possibly represents a new evolutionary lineage within the group of cyanophages infecting filamentous cyanobacteria, which form a separate cluster from phages infecting unicellular cyanobacteria. CL 131 encodes a putative type V-U2 CRISPR-Cas system with one spacer (out of 10) targeting a DNA primase pseudogene in a cyanobacterium and a putative type II toxin-antitoxin system, consisting of a GNAT family N-acetyltransferase and a protein of unknown function containing the PRK09726 domain (characteristic of HipB antitoxins). Comparison of CL 131 proteins to reads from Baltic Sea and other available fresh- and brackish-water metagenomes and analysis of CRISPR-Cas arrays in publicly available A. flos-aquae genomes demonstrated that phages similar to CL 131 are present and dynamic in the Baltic Sea and share a common history with their hosts dating back at least several decades. In addition, different CRISPR-Cas systems within individual A. flos-aquae genomes targeted several sequences in the CL 131 genome, including genes related to virion structure and morphogenesis. Altogether, these findings revealed new genomic information for exploring viral diversity and provide a model system for investigation of virus-host interactions in filamentous cyanobacteria.IMPORTANCE The genomic characterization of novel cyanophage vB_AphaS-CL131 and the analysis of its genomic features in the context of other viruses, metagenomic data, and host CRISPR-Cas systems contribute toward a better understanding of aquatic viral diversity and distribution in general and of brackish-water cyanophages infecting filamentous diazotrophic cyanobacteria in the Baltic Sea in particular. The results of this study revealed previously undescribed features of cyanophage genomes (e.g., self-excising intein-containing putative dCTP deaminase and putative cyanophage-encoded CRISPR-Cas and toxin-antitoxin systems) and can therefore be used to predict potential interactions between bloom-forming cyanobacteria and their cyanophages.

Dataset Information

Nitrogen Flow in Diazotrophic Cyanobacterium Aphanizomenon flos-aquae Is Altered by Cyanophage Infection.

Publications

Nitrogen Flow in Diazotrophic Cyanobacterium <i>Aphanizomenon flos-aquae</i> Is Altered by Cyanophage Infection.

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