Thermal history influences the recovery of phototrophic biofilms exposed to agricultural run-off in intermittent rivers

The response of microbial communities to disturbances may be controlled by the past environmental conditions, through their legacy effect. In intermittent rivers, the fixed microorganisms, such as phototrophic biofilms, are exposed to variable environmental conditions, including changes in water chemistry, hydrodynamics and, in some cases water temperature. The latter may be particularly affected by the increasing frequency of summer heat waves. Our objective was therefore to assess the legacy effect of warming on phototrophic biofilms during a flow intermittency sequence. Our main hypotheses were that the thermal history of biofilms determines (i) the community trajectory after rewetting and (ii) its resistance and resilience to a new disturbance. To test these hypotheses, we exposed phototrophic biofilms grown in the lab to a flow intermittency sequence (1 week no flow / 12 weeks no water) at two contrasted temperatures (22 °C and 32 °C). After rewetting (22 °C), some of the biofilms were exposed for 1 week to a new disturbance, i.e. a contaminant mimicking agricultural run-off (nitrate, copper, insecticide, herbicide, fungicide). The structure (pigments, elementary composition, extracellular polymeric substances, prokaryotic composition) and functioning (respiration, photosynthesis, functional diversity) of the biofilms were measured at the end of the contamination, and after 1 and 3 weeks of recovery without contaminant. Our results unexpectedly show that one week after rewetting the "warmed" biofilms were less heterotrophic than the "non-warmed" biofilms. This effect was transitory, although the prokaryotic composition of the biofilms still diverged 4 weeks after rewetting. The legacy effect of warming was an increased sensitivity of the biofilms to the complex contaminant, especially at the highest concentrations. This legacy effect decreased with time for the general structure and functioning of the biofilms, but persisted for the prokaryotic composition. These findings highlight the importance of historical conditions, and particularly thermal history, in the ability of microbial communities to respond to disturbances.