• Antarctica;
  • benthic cyanobacteria;
  • photosynthesis;
  • psychrophile;
  • psychrotolerance

Oscillatorian cyanobacteria dominate benthic microbial mat communities in many polar freshwater ecosystems. Capable of growth at low temperatures, all benthic polar oscillatorians characterized to date are psychrotolerant (growth optima > 15° C) as opposed to psychrophilic (growth optima ≤ 15° C). Here, psychrophilic oscillatorians isolated from meltwater ponds on Antarctica's McMurdo Ice Shelf are described. Growth and photosynthetic rates were investigated at multiple temperatures, and compared with those of a psychrotolerant isolate from the same region. Two isolates showed a growth maximum at 8° C, with rates of 0.12 and 0.08 doublings·d1, respectively. Neither displayed detectable growth at 24° C. The psychrotolerant isolate showed almost imperceptible growth at 4° C and a rate of 0.9 doublings·d1 at its optimal temperature of ∼23° C. In both photosynthesis versus irradiance and photosynthesis versus temperature experiments, exponentially growing cultures were acclimated for 14 days at 3, 8, 12, 20, and 24° C under saturating light intensity, and [14C] photoincorporation rates were measured. Psychrophilic isolates acclimated at 8° C showed greatest photosynthetic rates; those acclimated at 3° C were capable of active photosynthesis, but photoincorporation was not detected in cells acclimated at 20 and 24° C, because these isolates were not viable after 14 days at those temperatures. The psychrotolerant isolate, conversely, displayed maximum photosynthetic rates at 24° C, though photoincorporation was actively occurring at 3° C. Within acclimation temperature treatments, short-term photosynthetic rates increased with increasing incubation temperature for both psychrophilic and psychrotolerant isolates. These results indicate the importance of temperature acclimation before assays when determining optimal physiological temperatures. All isolates displayed photosynthetic saturation at low light levels (<128 μmol·m2·s1) but were not photoinhibited at the highest light treatment (233 μmol·m2·s1). Field studies examining the impact of temperature on photosynthetic responses of intact benthic mats, under natural solar irradiance, showed the mat communities to be actively photosynthesizing from 2 to 20° C, with maximum photoincorporation at 20° C, as well as capable of a rapid response to an increase in temperature. The rarity of psychrophilic cyanobacteria, relative to psychrotolerant strains, may be due to their extremely slow growth rates and inability to take advantage of occasional excursions to higher temperatures. We suggest an evolutionary scenario in which psychrophilic strains, or their most recent common ancestor, lost the ability to grow at higher temperatures while maintaining a broad tolerance for fluctuations in other physical and chemical parameters that define shallow meltwater Antarctic ecosystems.