Toxin-Antitoxin Systems in Estuarine Synechococcus Strain CB0101 and Their Transcriptomic Responses to Environmental Stressors

David Marsan,Daniel Fucich,Feng Chen,Allen Place

doi:10.3389/fmicb.2017.01213

Abstract

Bacterial toxin–antitoxin (TA) systems are genetic elements composed of a toxin gene and its cognate antitoxin, with the ability to regulate growth. TA systems have not previously been reported in marine Synechococcus or Prochlorococcus. Here we report the finding of seven TA system pairs (Type II) in the estuarine Synechococcus CB0101, and their responses of these TA genes to under different stress conditions, which include; nitrogen and phosphate starvation, phage infection, zinc toxicity, and photo-oxidation. Database searches discovered that eight other marine Synechococcus strains also contain at least one TA pair but none were found in Prochlorococcus. We demonstrate that the relB/relE TA pair was active and resulted in RNA degradation when CB0101 was under oxidative stress caused by either zinc toxicity or high light intensities, but the growth inhibition was released when the stress was removed. Having TA systems allows Synechococcus CB0101 to adapt to the low light and highly variable environments in the Chesapeake Bay. We propose that TA systems could be more important for picocyanobacteria living in the freshwater and estuarine environments compared to those living in the open ocean.

Highlights

Cyanobacteria are widely distributed in diverse habitats and they are able to adapt to variable and even extreme environments (Tandeau de Marsac and Houmard, 1993)
Significant hits among proteins encoded in these genomes were classified as toxins or antitoxins; in the case of multiple matches to different TA families, the protein was assigned according to the highest-scoring match TA query
Co-directed genes with adjacent chromosome locations belonging to different toxin/antitoxin families were recorded as a TA pair

Summary

Introduction

Cyanobacteria are widely distributed in diverse habitats and they are able to adapt to variable and even extreme environments (Tandeau de Marsac and Houmard, 1993). Estuaries are among the most productive yet variable aquatic environments on Earth. Mixing of fresh and marine waters provides strong environmental gradients to the cyanobacteria living in these ecosystems. Estuarine cyanobacteria (e.g., Synechococcus) contribute significantly to global primary production and are at the interface of direct anthropogenic affects (Ray et al, 1989; Affronti and Marshall, 1993; Iriarte and Purdie, 1994). The bioavailability of nutrients (e.g., N and P), light intensity, and trace metals (e.g., Fe and Zn) are highly variable. Due to the complex geochemistry of these compounds and physical dynamics, understanding cyanobacterial response to the estuarine environment is important toward understanding the function of ecosystems

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