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.
Highlights
Biological nitrogen (N2) fixation is an important process of the global biogeochemical cycles, considerably replenishing N losses to denitrification and anaerobic ammonium oxidation (Deutsch et al, 2007), and sustaining carbon export and sequestration in the ecosystemN2 Fixation During Cyanophage Infection (Karl et al, 2012)
Six hours after cyanophage addition, the number of CL 131 cyanophages decreased to ∼73% of its initial numbers, indicating that about 1/4 of all cyanophages in the stock adsorbed to its host cells
We described the effect of cyanophage infection on diazotrophic activity and N flow in the ecologically relevant heterocytous cyanobacterium A. flos-aquae
Summary
Biological nitrogen (N2) fixation (conversion of dissolved N2 gas into ammonia by microorganisms) is an important process of the global biogeochemical cycles, considerably replenishing N losses to denitrification and anaerobic ammonium oxidation (Deutsch et al, 2007), and sustaining carbon export and sequestration in the ecosystemN2 Fixation During Cyanophage Infection (Karl et al, 2012). Lysis of the infected cells and release of dissolved organic and inorganic nitrogen (viral shunt; Wilhelm and Suttle, 1999) were shown to induce structural and functional changes in co-occurring microbial communities and promoted pelagic production due to increased remineralization of the released nutrients (Shelford et al, 2012). These examples suggest that viral infection and lysis can directly modulate N transformations in the ecosystems. From the perspective of atmospheric nitrogen dynamics in diazotrophic cyanobacteria, one could hypothesize that infection by viruses can induce alterations in (i) nitrogen assimilation (N2 fixation) and (ii) release (ammonium) rates, due to, for example, metabolic reprogramming of the host cells (Doron et al, 2016) as well as (iii) redistribution of N within the infected cells by redirecting intracellular nutrient pool toward production of new virions (Ankrah et al, 2014)
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