The dynamics of biofilm bacterial communities is driven by flow wax and wane in a temporary stream

Biofilm communities are exposed to long periods of desiccation in temporary streams. We investigated how water flow intermittency affected the bacterial community structure colonizing three different streambed compartments in a Mediterranean stream. Massive parallel sequencing revealed different bacterial communities in biofilms from sand sediments and cobbles. Bacterial communities were similar (62% of shared operational taxonomic units) in the epipsammic and hyporheic biofilms, and more diverse than those in the epilithic biofilms. The non-flow phase caused a decrease of bacterial diversity in the biofilms, when communities included only bacterial taxa assumed to be adapted to water stress. The most sensitive bacterial communities to flow intermittency were in the epilithic, where the exposure to physical stress was the highest. In sand sediments a wide group of bacterial taxa was tolerant to desiccation. During non-flow the proliferation of opportunistic taxa in the superficial compartments evidenced the biological link with the terrestrial environment. Bacterial communities better tolerate rewetting than desiccation, since a major number of taxa tolerant to rewetting occurred in all biofilms. Overall, bacterial communities in sandy compartments showed higher resistance to flow intermittency than those in epilithic biofilms. Droughts are severely increasing in temperate regions worldwide and are usually associated with temporal and spatial increases of non-flow periods in streams and rivers. As a result, many systems become temporary, with unknown biogeochemical and ecological consequences for biodiversity and ecosystem functioning (Acuña et al. 2014). Particularly important are the non-flow and the flow recovery periods, when the system experiences desiccation and rewetting, respectively. These periods affect the biota survival and functioning in the stream and promote the selection of welladapted communities. In streambed sediments, microbial communities are directly affected by desiccation and rewetting (Amalfitano et al. 2008; Zoppini and Marxsen 2011; Timoner et al. 2012). Prokaryotes inhabiting these sediments play a pivotal role in the production and degradation of organic matter and nutrient cycling (Battin et al. 2003). Bacteria colonize all streambed substrata (mainly cobbles or sand sediments), and together with other microorganisms (archaea, algae, fungi, and protozoa) make part of biofilms. The bacterial community structure and functioning is related to environmental factors such as resource availability and temperature, but also to the water content in the sediments (Zeglin et al. 2011). Flow intermittency may therefore cause changes in the bacterial community composition of biofilms (Rees et al. 2006; Amalfitano et al. 2008; Febria et al. 2011), indicating that these communities respond to desiccation. Studies in soil and tidal sediments also show prominent changes in bacterial communities subjected to desiccation and rewetting (Fierer et al. 2003; McKew et al. 2011). During the non-flow phase, bacterial richness and diversity decrease, and only a few bacterial taxa surviving desiccation dominate (Rees et al. 2006; Febria et al. 2011). Changes in the community composition associated with desiccation could result both from a selection of the most resistant taxa (Evans and Wallenstein 2014), and from the colonization by immigrant and tolerant taxa (Fazi et al. 2008). Biofilm functioning, assessed through the ability of organic matter degradation (extracellular enzyme activities) decreases due to flow intermittency (Zoppini and Marxsen 2011) but does not disappear (Timoner et al. 2012). Further, the biofilm community structure and function rapidly recover after flow resumption (Rees et al. 2006; Zoppini and Marxsen 2011; Timoner et al. 2012). These are evidence that bacterial communities in temporary streams are able to thrive and function by adapting to the desiccation and rewetting cycles (Evans and Wallenstein 2014). The present study aims to understand the mechanisms associated with the dynamics of bacterial communities during flow intermittency, by analyzing the specific responses of bacterial communities in the epilithic, epipsammic, and hyporheic biofilms. We conducted a detailed profiling of these bacterial communities through pyrotag sequencing of the small subunit of the ribosomal ribonucleic acid (rRNA) gene. We hypothesized that: (1) the effects of flow intermittency would be more pronounced and long-lasting on the epilithic bacterial community, because of the harsher environmental conditions (low water content, high light irradiances and air temperatures) occurring during the non-flow phase. (2) Water flow wane would drive a selection towards desiccationresistant bacteria from the taxa already present during the flowing period. Accordingly, we would also expect that flow resumption would restore bacterial species prevalent before desiccation. (3) Bacterial taxa from the nearby terrestrial environment could perform as active colonizers in the more superficial streambed substrata, given the proximity between * Corresponding author: [email protected] Limnol. Oceanogr., 59(6), 2014, 2057–2067 E 2014, by the Association for the Sciences of Limnology and Oceanography, Inc. doi:10.4319/lo.2014.59.6.2057