Abstract

Microbial communities inhabiting high-altitude spring ecosystems are subjected to extreme changes in solar irradiance and temperature throughout the diel cycle. Here, using 16S rRNA gene tag pyrosequencing (cDNA) we determined the composition of actively transcribing bacteria from spring waters experimentally exposed through the day (morning, noon, and afternoon) to variable levels of solar radiation and light quality, and evaluated their influence on nutrient recycling. Solar irradiance, temperature, and changes in nutrient dynamics were associated with changes in the active bacterial community structure, predominantly by Cyanobacteria, Verrucomicrobia, Proteobacteria, and 35 other Phyla, including the recently described Candidate Phyla Radiation (e.g., Parcubacteria, Gracilibacteria, OP3, TM6, SR1). Diversity increased at noon, when the highest irradiances were measured (3.3–3.9 H′, 1125 W m-2) compared to morning and afternoon (0.6–2.8 H′). This shift was associated with a decrease in the contribution to pyrolibraries by Cyanobacteria and an increase of Proteobacteria and other initially low frequently and rare bacteria phyla (< 0.5%) in the pyrolibraries. A potential increase in the activity of Cyanobacteria and other phototrophic groups, e.g., Rhodobacterales, was observed and associated with UVR, suggesting the presence of photo-activated repair mechanisms to resist high levels of solar radiation. In addition, the percentage contribution of cyanobacterial sequences in the afternoon was similar to those recorded in the morning. The shifts in the contribution by Cyanobacteria also influenced the rate of change in nitrate, nitrite, and phosphate, highlighted by a high level of nitrate accumulation during hours of high radiation and temperature associated with nitrifying bacteria activity. We did not detect ammonia or nitrite oxidizing bacteria in situ, but both functional groups (Nitrosomona and Nitrospira) appeared mainly in pyrolibraries generated from dark incubations. In total, our results reveal that both the structure and the diversity of the active bacteria community was extremely dynamic through the day, and showed marked shifts in composition that influenced nutrient recycling, highlighting how abiotic variation affects potential ecosystem functioning.

Highlights

  • Cyanobacteria, Verrucomicrobia, Proteobacteria, and the non- amplified Euryarchaeota (Methanosarcinales) were the most active phyla detected in situ

  • Our findings based on 16S rRNA pyrosequencing supports previous studies and given that our results originate from cDNA indicate that wide diversity of phyla previously identified are present, and potentially active

  • The in situ active bacterial community displayed marked changes associated with both time and experimental treatments: these shifts are clearly displayed through both clustering and Principal Coordinates Analysis (PCoA) analyses (Figures 2 and 5)

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Summary

Introduction

The Salar de Huasco is largely groundwater fed, and upwells via a limited number of springs, which generate a wetland habitat, characterized by complex pond and pool systems surrounded by vascular plants forming peatland, locally referred to as bofedales” with the water flowing into a permanent shallow lake (de a Fuente and Niño, 2010) Aquatic life in this and other similar high-altitude ecosystems in the Andes is adapted to extreme conditions, and faces temporal changes in salinity and nutrient availability such as nitrogen across seasonal and inter-annual scales (MarquezGarcia et al, 2009). Microbial life in these ecosystems is notably highly diverse, characterized by novel groups of prokaryotes, and includes the conspicuous presence of microbial mats (Dorador et al, 2008a,b, 2009, 2013). Highland aquatic ecosystems such as the Altiplano and the high lakes of the Tibetan plateau represent hotspots of microbial life, and can be considered as model ecosystems to study the response of microorganisms to environmental gradients (Jiang et al, 2009; Hu et al, 2010; Kang et al, 2010; Albarracin et al, 2015)

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