Biofilm formation and cell plasticity drive diazotrophy in an anoxygenic phototrophic bacterium

Non-cyanobacterial diazotrophs (NCDs) are widespread and active in marine waters. The carbon and low-oxygen (O-2) conditions required for their N-2 fixation may be encountered on marine particles, while a putative role of light remains uninvestigated. This study explored factors that regulate N-2 fixation in Rhodopseudomonas sp. BAL398-a anoxygenic phototrophic bacterium isolated from low-salinity surface waters. Light (250 mu mol photons m(-2) s(-1)) and anoxia (0 mu M O-2) stimulated growth and N-2 fixation; however, diazotrophy in light was dependent on high organic carbon levels (35 mM, glucose:succinate). Immunolabeling revealed that cellular nitrogenase levels increased with light, decreasing inorganic nitrogen (N) and ambient O-2 (250 mu M). Light and O-2 stimulated motility and biofilm formation on surfaces, and N-2 fixation rates increased compared to the control treatment. N-2 fixation rates were positively correlated with the formation of rosette-like cellular structures, and an increased concentration of nitrogenase was observed toward the center of these structures, which increased their occurrence 600 times when cultures reached maximum N-2 fixation rates vs when they had low rates. Interestingly, N-2 fixation was not completely inhibited under oxic conditions and was accompanied by increased formation of capsules and cysts. Rosettes, as well as capsules and cysts, may thus serve as protection against O-2. Our study reveals the physiological adaptations that underlie N-2 fixation in an anoxygenic phototroph, emphasizing the significance of biofilm formation for utilizing light and fixing N-2 under oxic conditions, and underscores the need for deciphering the importance of light for marine NCDs.

Automated summary

This study examined the factors that regulate nitrogen fixation in an anoxygenic phototrophic bacterium and found that light and anoxia stimulated nitrogen fixation. The study also revealed the importance of biofilm formation for nitrogen fixation under oxic conditions. These findings highlight the physiological adaptations and the role of light in marine non-cyanobacterial diazotrophs.