Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community

Pratibha Panwar,Nicole Shapiro,David Páez-Espino,Simon Roux,Alyce M Hancock,Frederik Schulz,Emiley A Eloe-Fadrosh,James Bevington,Tanja Woyke,Nikos C Kyrpides,Stephen Nayfach,Michelle A Allen,Sarah Brazendale,Maureen Berg,I-Min A Chen,Timothy J Williams,Ricardo Cavicchioli,Marcel Huntemann

doi:10.1186/s40168-020-00889-8

Pratibha Panwar, Nicole Shapiro + Show 16 more

Open Access

https://doi.org/10.1186/s40168-020-00889-8

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Abstract

BackgroundCold environments dominate the Earth’s biosphere and microbial activity drives ecosystem processes thereby contributing greatly to global biogeochemical cycles. Polar environments differ to all other cold environments by experiencing 24-h sunlight in summer and no sunlight in winter. The Vestfold Hills in East Antarctica contains hundreds of lakes that have evolved from a marine origin only 3000–7000 years ago. Ace Lake is a meromictic (stratified) lake from this region that has been intensively studied since the 1970s. Here, a total of 120 metagenomes representing a seasonal cycle and four summers spanning a 10-year period were analyzed to determine the effects of the polar light cycle on microbial-driven nutrient cycles.ResultsThe lake system is characterized by complex sulfur and hydrogen cycling, especially in the anoxic layers, with multiple mechanisms for the breakdown of biopolymers present throughout the water column. The two most abundant taxa are phototrophs (green sulfur bacteria and cyanobacteria) that are highly influenced by the seasonal availability of sunlight. The extent of the Chlorobium biomass thriving at the interface in summer was captured in underwater video footage. The Chlorobium abundance dropped from up to 83% in summer to 6% in winter and 1% in spring, before rebounding to high levels. Predicted Chlorobium viruses and cyanophage were also abundant, but their levels did not negatively correlate with their hosts.ConclusionOver-wintering expeditions in Antarctica are logistically challenging, meaning insight into winter processes has been inferred from limited data. Here, we found that in contrast to chemolithoautotrophic carbon fixation potential of Southern Ocean Thaumarchaeota, this marine-derived lake evolved a reliance on photosynthesis. While viruses associated with phototrophs also have high seasonal abundance, the negative impact of viral infection on host growth appeared to be limited. The microbial community as a whole appears to have developed a capacity to generate biomass and remineralize nutrients, sufficient to sustain itself between two rounds of sunlight-driven summer-activity. In addition, this unique metagenome dataset provides considerable opportunity for future interrogation of eukaryotes and their viruses, abundant uncharacterized taxa (i.e. dark matter), and for testing hypotheses about endemic species in polar aquatic ecosystems.3rEAa4a8EPvdQSJ1TDqSyzVideo

Highlights

Cold environments dominate the Earth’s biosphere and microbial activity drives ecosystem processes thereby contributing greatly to global biogeochemical cycles
The microbial community in Ace Lake is defined by a marine-seed population that was isolated from the Southern Ocean ~ 5000 year ago [10]
green sulfur bacteria (GSB) are present in a number of stratified aquatic systems in the Vestfold Hills [15] and are abundant in some Arctic lakes (e.g. Pelodictyon in Lake A [73]), but have not been reported to be generally abundant in Antarctic aquatic systems

Summary

Introduction

Cold environments dominate the Earth’s biosphere and microbial activity drives ecosystem processes thereby contributing greatly to global biogeochemical cycles. Polar environments differ to all other cold environments by experiencing 24-h sunlight in summer and no sunlight in winter. The cold biosphere includes distinct biomes: the depths of the global ocean, alpine regions, and polar regions. Each of these cold biomes are characterized by specific abiotic factors. Polar regions are perennially cold and subject to a polar light regime where summer brings 24-h sunlight, winter no sunlight, and autumn/spring occurs within a compressed time frame. Alpine regions such as parts of the Tibetan Plateau exhibit a similar range of annual temperatures to parts of Antarctica, but are exposed to a light cycle reflective of their latitude. Understanding food web structures and biogeochemical cycles in cold environments requires an appreciation of the relevant environmental factors [2, 3]

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