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

Abstract Background 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 win...

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Main Authors: Panwar, Pratibha, Allen, Michelle A., Williams, Timothy J., Hancock, Alyce M., Brazendale, Sarah, Bevington, James, Roux, Simon, Páez-Espino, David, Nayfach, Stephen, Berg, Maureen, Schulz, Frederik, I-Min A. Chen, Huntemann, Marcel, Shapiro, Nicole, Kyrpides, Nikos C., Woyke, Tanja, Emiley A. Eloe-Fadrosh, Cavicchioli, Ricardo
Format: Article in Journal/Newspaper
Language:unknown
Published: figshare 2021
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.5086955.v2
https://springernature.figshare.com/collections/Influence_of_the_polar_light_cycle_on_seasonal_dynamics_of_an_Antarctic_lake_microbial_community/5086955/2
id ftdatacite:10.6084/m9.figshare.c.5086955.v2
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.5086955.v2 2023-05-15T13:51:37+02:00 Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community Panwar, Pratibha Allen, Michelle A. Williams, Timothy J. Hancock, Alyce M. Brazendale, Sarah Bevington, James Roux, Simon Páez-Espino, David Nayfach, Stephen Berg, Maureen Schulz, Frederik I-Min A. Chen Huntemann, Marcel Shapiro, Nicole Kyrpides, Nikos C. Woyke, Tanja Emiley A. Eloe-Fadrosh Cavicchioli, Ricardo 2021 https://dx.doi.org/10.6084/m9.figshare.c.5086955.v2 https://springernature.figshare.com/collections/Influence_of_the_polar_light_cycle_on_seasonal_dynamics_of_an_Antarctic_lake_microbial_community/5086955/2 unknown figshare https://dx.doi.org/10.1186/s40168-020-00889-8 https://dx.doi.org/10.6084/m9.figshare.c.5086955 Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode cc-by-4.0 CC-BY Microbiology FOS Biological sciences Ecology Collection article 2021 ftdatacite https://doi.org/10.6084/m9.figshare.c.5086955.v2 https://doi.org/10.1186/s40168-020-00889-8 https://doi.org/10.6084/m9.figshare.c.5086955 2021-11-05T12:55:41Z Abstract Background 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 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. Results The 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. Conclusion Over-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. Video Abstract Article in Journal/Newspaper Antarc* Antarctic Antarctica East Antarctica Southern Ocean DataCite Metadata Store (German National Library of Science and Technology) Antarctic Southern Ocean East Antarctica Vestfold Hills Vestfold Ace Lake ENVELOPE(78.188,78.188,-68.472,-68.472)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Microbiology
FOS Biological sciences
Ecology
spellingShingle Microbiology
FOS Biological sciences
Ecology
Panwar, Pratibha
Allen, Michelle A.
Williams, Timothy J.
Hancock, Alyce M.
Brazendale, Sarah
Bevington, James
Roux, Simon
Páez-Espino, David
Nayfach, Stephen
Berg, Maureen
Schulz, Frederik
I-Min A. Chen
Huntemann, Marcel
Shapiro, Nicole
Kyrpides, Nikos C.
Woyke, Tanja
Emiley A. Eloe-Fadrosh
Cavicchioli, Ricardo
Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
topic_facet Microbiology
FOS Biological sciences
Ecology
description Abstract Background 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 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. Results The 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. Conclusion Over-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. Video Abstract
format Article in Journal/Newspaper
author Panwar, Pratibha
Allen, Michelle A.
Williams, Timothy J.
Hancock, Alyce M.
Brazendale, Sarah
Bevington, James
Roux, Simon
Páez-Espino, David
Nayfach, Stephen
Berg, Maureen
Schulz, Frederik
I-Min A. Chen
Huntemann, Marcel
Shapiro, Nicole
Kyrpides, Nikos C.
Woyke, Tanja
Emiley A. Eloe-Fadrosh
Cavicchioli, Ricardo
author_facet Panwar, Pratibha
Allen, Michelle A.
Williams, Timothy J.
Hancock, Alyce M.
Brazendale, Sarah
Bevington, James
Roux, Simon
Páez-Espino, David
Nayfach, Stephen
Berg, Maureen
Schulz, Frederik
I-Min A. Chen
Huntemann, Marcel
Shapiro, Nicole
Kyrpides, Nikos C.
Woyke, Tanja
Emiley A. Eloe-Fadrosh
Cavicchioli, Ricardo
author_sort Panwar, Pratibha
title Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
title_short Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
title_full Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
title_fullStr Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
title_full_unstemmed Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community
title_sort influence of the polar light cycle on seasonal dynamics of an antarctic lake microbial community
publisher figshare
publishDate 2021
url https://dx.doi.org/10.6084/m9.figshare.c.5086955.v2
https://springernature.figshare.com/collections/Influence_of_the_polar_light_cycle_on_seasonal_dynamics_of_an_Antarctic_lake_microbial_community/5086955/2
long_lat ENVELOPE(78.188,78.188,-68.472,-68.472)
geographic Antarctic
Southern Ocean
East Antarctica
Vestfold Hills
Vestfold
Ace Lake
geographic_facet Antarctic
Southern Ocean
East Antarctica
Vestfold Hills
Vestfold
Ace Lake
genre Antarc*
Antarctic
Antarctica
East Antarctica
Southern Ocean
genre_facet Antarc*
Antarctic
Antarctica
East Antarctica
Southern Ocean
op_relation https://dx.doi.org/10.1186/s40168-020-00889-8
https://dx.doi.org/10.6084/m9.figshare.c.5086955
op_rights Creative Commons Attribution 4.0 International
https://creativecommons.org/licenses/by/4.0/legalcode
cc-by-4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.5086955.v2
https://doi.org/10.1186/s40168-020-00889-8
https://doi.org/10.6084/m9.figshare.c.5086955
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