Abstract
Microbial mats are ubiquitous in polar freshwater ecosystems and sustain high concentrations of biomass despite the extreme seasonal variations in light and temperature. Here we aimed to resolve genomic adaptations for light-harvesting, bright-light protection, and carbon flow in mats that undergo seasonal freeze-up. To bracket a range of communities in shallow water habitats, we sampled cyanobacterial mats in the thawed littoral zone of two lakes situated at the northern and southern limits of the Canadian Arctic permafrost zone. We applied a multiphasic approach using pigment profiles from high performance liquid chromatography, Illumina MiSeq sequencing of the 16S and 18S rRNA genes, and metagenomic analysis. The mats shared a taxonomic and functional core microbiome, dominated by oxygenic cyanobacteria with light-harvesting and photoprotective pigments, bacteria with bacteriochlorophyll, and bacteria with light-driven Type I rhodopsins. Organisms able to use light for energy related processes represented up to 85% of the total microbial community, with 15–30% attributable to cyanobacteria and 55–70% attributable to other bacteria. The proportion of genes involved in anaplerotic CO2 fixation was greater than for genes associated with oxygenic photosynthesis. Diverse heterotrophic bacteria, eukaryotes (including metazoans and fungi) and viruses co-occurred in both communities. The results indicate a broad range of strategies for capturing sunlight and CO2, and for the subsequent flow of energy and carbon in these complex, light-driven microbial ecosystems.
Highlights
Cyanobacterial mats are found in many temperate environments, but are often restricted to hypersaline or hydrothermal environments (Allewalt et al, 2006; Ley et al, 2006) where environmental conditions limit grazer diversity and activity (Stanish et al, 2013; Stal et al, 2017)
The microbial mat community composition from high Arctic Ward Hunt Lake and low Arctic Lake 9K were determined by both rRNA gene amplicon sequencing and metagenomic analysis
The vast majority (96.6% overall) of metagenomic ribosomal genes from all samples were affiliated with Bacteria, with Eukaryota accounting for 4.4 ± 0.6% of the rRNA reads
Summary
Cyanobacterial mats are found in many temperate environments, but are often restricted to hypersaline or hydrothermal environments (Allewalt et al, 2006; Ley et al, 2006) where environmental conditions limit grazer diversity and activity (Stanish et al, 2013; Stal et al, 2017). Microbial mats must contend with the extreme conditions. Comparative analyses of microbial mat communities from high latitudes with those from other regions suggests selection for microorganisms with metabolic pathways that enable survival under conditions such as prolonged freezing, winter darkness and continuous bright light exposure in summer (White et al, 2015; Kleinteich et al, 2017). Polar microbial mats were initially thought to be relatively simple associations of filamentous cyanobacteria embedded within a mucopolysaccharide gel (Vincent, 1988). Co-occurring taxa include many bacterial lineages, autotrophic and heterotrophic protists, fungi, metazoans, and viruses (Vincent et al, 2009; Jungblut et al, 2012; Peeters et al, 2012), suggesting that the mats are complex microbial ecosystems and should be considered as functional consortia. Amplicon and metagenomic surveys have reported a large contribution of proteobacterial lineages within polar mat communities (Bottos et al, 2008; Varin et al, 2010; Lionard et al, 2012; Mohit et al, 2017)
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