Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes

Abstract

Northern lakes are ice-covered for a large part of the year, yet our understanding of microbial diversity and activity during winter lags behind that of the ice-free period. In this study, we investigated under-ice diversity and metabolism of Verrucomicrobia in seasonally ice-covered lakes in temperate and boreal regions of Quebec, Canada using 16S rRNA sequencing, metagenomics and metatranscriptomics. Verrucomicrobia, particularly the V1, V3 and V4 subdivisions, were abundant during ice-covered periods. A diversity of Verrucomicrobia genomes were reconstructed from Quebec lake metagenomes. Several genomes were associated with the ice-covered period and were represented in winter metatranscriptomes, supporting the notion that Verrucomicrobia are metabolically active under ice. Verrucomicrobia transcriptome analysis revealed a range of metabolisms potentially occurring under ice, including carbohydrate degradation, glycolate utilization, scavenging of chlorophyll degradation products, and urea use. Genes for aerobic sulfur and hydrogen oxidation were expressed, suggesting chemolithotrophy may be an adaptation to conditions where labile carbon may be limited. The expression of genes for flagella biosynthesis and chemotaxis was detected, suggesting Verrucomicrobia may be actively sensing and responding to winter nutrient pulses, such as phytoplankton blooms. These results increase our understanding on the diversity and metabolic processes occurring under ice in northern lakes ecosystems.© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.

Genome diversification in globally distributed novel marine Proteobacteria is linked to environmental adaptation

“…PhyH could hydroxylate the methyl-branched chain of phytanoyl-CoA and is required in the alpha-oxidation pathway of fatty acid metabolism to move the methyl-group from beta position to the alpha position 52 . Together with the metabolism of alcohol and aldehyde dehydrogenases and acyl-CoA synthetase, it is feasible for bacteria to transform phytol (a long-chain alcohol constituent of chlorophyll) to phytanoyl-CoA and pass the products downstream towards beta-oxidation and energy utilization 52, 53 . The exclusive distribution of PhyH in the non-photic zone clade implicates that this specific group could potentially scavenge the degradation products of chlorophyll for carbon and energy demand, which could possibly be of phytoplankton-origin from the upper ocean layers (e.g., deep chlorophyll maximum) 54 .…”

Annual bacterial community cycle in a seasonally ice‐covered river reflects environmental and climatic conditions

“…These long-held perceptions have led to the assumption that the cold season in shallow freshwater ecosystems is a "dormant season" in contrast to the warm "growing season". However, recent research has shown that the winter can be a season of important biological activity in freshwater ecosystems (Campbell et al 2005;Kankaala et al 2006;Bertilsson et al 2013;Hampton et al 2017;Tran et al 2018). Indeed, many biological processes persist throughout the winter while others initiate and develop at low temperatures.…”

“…As ice cover results in a lower availability of organic substrates from terrestrial input or phytoplankton, other energy and carbon sources, not restricted by ice cover, might be used by other organisms. Organic matter degradation, scavenging of decaying photosynthetic biomass and chemolithotrophic pathways have been identified in under-ice freshwater ecosystems, indicating that under-ice microbial communities may also contribute to carbon and energy cycling (Sundh et al 2005;Kankaala et al 2006;Tran et al 2018). Higher nitrogen and nitrate concentrations have been also frequently observed in freshwater ecosystems during the cold season (Suberkropp et al 1976;Hampton et al 2017), indicating changes in nitrogen consumers and producers as well as associated processes at low temperatures.…”

“…Although the number of studies investigating winter ecology in lakes is increasing (e.g., Sundh et al 2005;Kankaala et al 2006;Biži c-Ionescu et al 2014;Hampton et al 2017;Tran et al 2018), other inland waters, such as rivers and streams, remain poorly investigated. However, riverine ecosystems should not be considered as simple passive pipes but as biophysical reactors that could transform the geochemical compounds they transport and thus must be considered as important contributors to global biogeochemical cycles (Cole et al 2007;Tranvik et al 2009;Proia et al 2016).…”

Wide distribution of phage that infect freshwater SAR11 bacteria

“…To report the BLASTp hits in the IMG metagenomic datasets in this manuscript, we asked the Principal Investigators for each public dataset for their permission to report the results ( Supplementary Table 8 ). The data in these metagenomic datasets have been published (Denef et al 2016;Otten et al 2016;Pinto et al 2016;Colatriano et al 2018;Dalcin Martins et al 2018;Tran et al 2018;Daly et al 2019) , or are in preparation for publication (Davenport et al, in prep; Paver et al, in revision; Evans et al, in prep).…”