Novel autotrophic organisms contribute significantly to the internal carbon cycling potential of a boreal lake

Abstract

The authors declare no conflict of interest\n\nFunding sources: the Academy of Finland, Science for Life Laboratories, Tryggers Foundation, the Swedish Research Council VR and the Swedish Foundation for strategic research\n\nAbstractOxygen stratified lakes are typical for the boreal zone, and also a major source of greenhouse gas emissions in the region. Due to shallow light penetration, restricting the growth of phototrophic organisms, and large allochthonous organic carbon inputs from the catchment area, the lake metabolism is expected to be dominated by heterotrophic organisms. In this study we test this assumption and show that the potential for autotrophic carbon fixation and internal carbon cycling is high throughout the water column. Further, we show that during the summer stratification carbon fixation can exceed respiration in a boreal lake even below the euphotic zone. Metagenome assembled genomes and 16S profiling of a vertical transect of the lake revealed multiple organisms in oxygen depleted compartment belonging to novel or poorly characterized phyla. Many of these organisms were chemolithotrophic, deriving their energy from reactions related to sulfur, iron and nitrogen transformations. The community as well as the functions were stratified following the redox potentials. The autotrophic potential in the lake metagenome below the oxygenic zone was high, pointing towards a need for revising our concepts of internal carbon cycling in boreal lakes. Further, the importance of chemolithoautotrophy for the internal carbon cycling suggests that many predicted climate change associated changes in the physical properties of the lake, such as altered mixing patterns, likely have consequences for the whole lake metabolism even beyond the impact to the phototrophic community.\n\nImportanceAutotrophic organisms at the base of the food web are the only life form capable of turning inorganic carbon into organic form, facilitating the survival of all other organisms. In certain environments the autotrophic production is limited by environmental conditions and the food web is supported by carbon coming from outside the ecosystem. One such environment is stratified boreal lakes, which are one of the biggest sources of greenhouse gas emissions in the boreal region. Thus, carbon cycling in these habitats is of outmost importance for the future climate. Here we demonstrate a high potential for internal carbon cycling via phototrophic and novel chemolithotrophic organisms in the dark and anoxic layers of a boreal lake. Our results significantly increase our knowledge on the microbial communities and their metabolic potential in oxygen depleted freshwaters and help to understand and predict how climate change induced alterations could impact the lake carbon dynamics.