The surface and surroundings of microalgal cells (phycosphere) are critical interaction zones but have been difficult to functionally interrogate due to methodological limitations. We examined effects of phycosphere-associated bacteria for two biofuel-relevant microalgal species (Phaeodactylum tricornutum and Nannochloropsis salina) using stable isotope tracing and high spatial resolution mass spectrometry imaging (NanoSIMS) to quantify elemental exchanges at the single-cell level. Each algal species responded differently to bacterial attachment. In P. tricornutum, a high percentage of cells had attached bacteria (92%-98%, up to eight bacteria per alga) and fixed 64% more carbon with attached bacteria compared to axenic cells. In contrast, N. salina cells were less commonly associated with bacteria (42%-63%), harboured fewer bacteria per alga, and fixed 10% more carbon without attached bacteria compared to axenic cells. An uncultivated bacterium related to Haliscomenobacter sp. was identified as an effective mutualist; it increased carbon fixation when attached to P. tricornutum and incorporated 71% more algal-fixed carbon relative to other bacteria. Our results illustrate how phylogenetic identity and physical location of bacteria and algae facilitate diverse metabolic responses. Phycosphere-mediated, mutualistic chemical exchanges between autotrophs and heterotrophs may be a fruitful means to increase microalgal productivity for applied engineering efforts.
© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.