Quorum sensing between phylogenetically ancient Cyanobacteria and heterotrophic Bacteria in a simulated Mars atmosphere

Abstract

N-acyl homoserine lactone based quorum sensing (AHL-QS), a form of chemical communication and gene regulation in bacteria, was investigated in a Cyanobacteria-heterotroph consortium under contemporary terrestrial and simulated Mars conditions. Co-cultures of a deeply branching, phylogenetically ancient cyanobacterium, Gloeobacter violaceus, and its heterotrophic consortium were maintained in a simulated Mars atmosphere, i.e., atmospheric composition of high CO2-low O2 concentrations. First, the type and relative concentrations of AHLs produced by heterotrophic consortia were determined. Then, differential gene expression of co-cultures by RNA-seq was determined when 1) exogenous AHLs were applied to co-cultures and 2) under simulated Mars atmospheric conditions. The results show that G. violaceus, an early-Earth, photoautotrophic representative, and its heterotrophic consortium that commonly occur in epilithic, Mars-analog environments, 1) have a vast potential for AHL-QS, 2) show differential gene expression in response to Mars atmospheric conditions, as well as exposure to an AHL molecule. Differential gene expression by RNA-seq results reveals that there is significant differential expression of genes involved in cobalt uptake and phage tail assembly by G. violaceus, possibly in response to exogenous application of 3-oxo-C12-homoserine lactone (C12-oxo). This provides context for how microbial consortia in a Mars atmosphere may withstand environmental extremes through inter-species interactions, and informs future work on life’s persistence on Earth and potentially elsewhere in the Solar System. Ultimately, this project has shown that AHL-QS can be linked to an evolutionary timeline of cooperative microbial interactions, particularly in Cyanobacteria.