Abstract
ABSTRACTOxygen-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 an oxygen-depleted compartment belonging to novel or poorly characterized phyla. Many of these organisms were chemolithotrophic, potentially deriving their energy from reactions related to sulfur, iron, and nitrogen transformations. The community, as well as the functions, was stratified along the redox gradient. The autotrophic potential in the lake metagenome below the oxygenic zone was high, pointing toward 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 fluctuations 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.
Highlights
Oxygen-stratified lakes are typical for the boreal zone and a major source of greenhouse gas emissions in the region
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
The metabolic pathways and organisms that could be involved in autotrophic processes in the water column of the lake Alinen Mustajärvi were studied based on molecular and geochemical analyses from samples taken in 2013
Summary
Oxygen-stratified lakes are typical for the boreal zone and a major source of greenhouse gas emissions in the region. Water bodies smaller than 0.001 km contribute 40% of all methane emissions from inland waters [13] These small lakes and ponds are characterized by high concentrations of dissolved organic carbon (DOC) and shallow light penetration depth, which leads to steep stratification of oxygen and other electron acceptors and donors through most of the year. The microbial communities in these lakes may harbor organisms that have the potential for photoautotrophy under low light intensity [14, 16, 17] and for chemoautotrophy throughout the water column [9] These predictions are based on taxonomic information derived from 16S rRNA genes combined with functional gene inventories and genomic data of related cultivated representatives. This lack of a detailed metabolic picture limits our understanding of the functional potential of microbes in boreal lakes
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