Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier

Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. BChl and rhodopsin-based systems display contrasting characteristics in the size of coding operon, cost of b...

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Published in:mBio
Main Authors: Zeng, Yonghui, Chen, Xihan, Madsen, Anne Mette, Zervas, Athanasios, Nielsen, Tue Kjærgaard, Andrei, Adrian Stefan, Lund-Hansen, Lars Chresten, Liu, Yongqin, Hansen, Lars Hestbjerg
Format: Article in Journal/Newspaper
Language:English
Published: 2020
Subjects:
Online Access:https://pure.au.dk/portal/da/publications/potential-rhodopsin-and-bacteriochlorophyllbased-dual-phototrophy-in-a-high-arctic-glacier(9b4adc0f-7a32-46b1-af0f-33e37ed2d7fa).html
https://doi.org/10.1128/mBio.02641-20
http://www.scopus.com/inward/record.url?scp=85096815869&partnerID=8YFLogxK
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spelling ftuniaarhuspubl:oai:pure.atira.dk:publications/9b4adc0f-7a32-46b1-af0f-33e37ed2d7fa 2023-12-10T09:43:42+01:00 Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier Zeng, Yonghui Chen, Xihan Madsen, Anne Mette Zervas, Athanasios Nielsen, Tue Kjærgaard Andrei, Adrian Stefan Lund-Hansen, Lars Chresten Liu, Yongqin Hansen, Lars Hestbjerg 2020-11 https://pure.au.dk/portal/da/publications/potential-rhodopsin-and-bacteriochlorophyllbased-dual-phototrophy-in-a-high-arctic-glacier(9b4adc0f-7a32-46b1-af0f-33e37ed2d7fa).html https://doi.org/10.1128/mBio.02641-20 http://www.scopus.com/inward/record.url?scp=85096815869&partnerID=8YFLogxK eng eng https://pure.au.dk/portal/da/publications/potential-rhodopsin-and-bacteriochlorophyllbased-dual-phototrophy-in-a-high-arctic-glacier(9b4adc0f-7a32-46b1-af0f-33e37ed2d7fa).html info:eu-repo/semantics/openAccess Zeng , Y , Chen , X , Madsen , A M , Zervas , A , Nielsen , T K , Andrei , A S , Lund-Hansen , L C , Liu , Y & Hansen , L H 2020 , ' Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier ' , mBio , vol. 11 , no. 6 , e02641-20 , pp. 1-8 . https://doi.org/10.1128/mBio.02641-20 bacteriochlorophyll genome evolution glacial bacteria phototrophy rhodopsin article 2020 ftuniaarhuspubl https://doi.org/10.1128/mBio.02641-20 2023-11-16T00:00:23Z Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. BChl and rhodopsin-based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of phototrophy complementarily according to energy needs and environmental conditions. Here, we report four Tardiphaga sp. strains (Alphaproteobacteria) of monophyletic origin isolated from a high Arctic glacier in northeast Greenland (81.566° N, 16.363° W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfer (HOT) of the complete gene clusters encoding BChl- and xanthorhodopsin (XR)-based dual phototrophy. Two strains possess only a complete XR operon, while the other two strains have both a photosynthesis gene cluster and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and are located close to a tRNA gene, strongly signaling that a HOT event of the XR operon has occurred recently. Mining public genome databases and our high Arctic glacial and soil metagenomes revealed that phylogenetically diverse bacteria have the metabolic potential of performing BChl- and rhodopsin-based dual phototrophy. Our data provide new insights on how bacteria cope with the harsh and energy-deficient environment in surface glacier, possibly by maximizing the capability of exploiting solar energy.IMPORTANCE Over the course of evolution for billions of years, bacteria that are capable of light-driven energy production have occupied every corner of surface Earth where sunlight can reach. Only two general biological systems have evolved in bacteria to be capable of net energy conservation via light harvesting: ... Article in Journal/Newspaper Arctic Arctic glacier Greenland Aarhus University: Research Arctic Greenland mBio 11 6
institution Open Polar
collection Aarhus University: Research
op_collection_id ftuniaarhuspubl
language English
topic bacteriochlorophyll
genome evolution
glacial bacteria
phototrophy
rhodopsin
spellingShingle bacteriochlorophyll
genome evolution
glacial bacteria
phototrophy
rhodopsin
Zeng, Yonghui
Chen, Xihan
Madsen, Anne Mette
Zervas, Athanasios
Nielsen, Tue Kjærgaard
Andrei, Adrian Stefan
Lund-Hansen, Lars Chresten
Liu, Yongqin
Hansen, Lars Hestbjerg
Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier
topic_facet bacteriochlorophyll
genome evolution
glacial bacteria
phototrophy
rhodopsin
description Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. BChl and rhodopsin-based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of phototrophy complementarily according to energy needs and environmental conditions. Here, we report four Tardiphaga sp. strains (Alphaproteobacteria) of monophyletic origin isolated from a high Arctic glacier in northeast Greenland (81.566° N, 16.363° W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfer (HOT) of the complete gene clusters encoding BChl- and xanthorhodopsin (XR)-based dual phototrophy. Two strains possess only a complete XR operon, while the other two strains have both a photosynthesis gene cluster and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and are located close to a tRNA gene, strongly signaling that a HOT event of the XR operon has occurred recently. Mining public genome databases and our high Arctic glacial and soil metagenomes revealed that phylogenetically diverse bacteria have the metabolic potential of performing BChl- and rhodopsin-based dual phototrophy. Our data provide new insights on how bacteria cope with the harsh and energy-deficient environment in surface glacier, possibly by maximizing the capability of exploiting solar energy.IMPORTANCE Over the course of evolution for billions of years, bacteria that are capable of light-driven energy production have occupied every corner of surface Earth where sunlight can reach. Only two general biological systems have evolved in bacteria to be capable of net energy conservation via light harvesting: ...
format Article in Journal/Newspaper
author Zeng, Yonghui
Chen, Xihan
Madsen, Anne Mette
Zervas, Athanasios
Nielsen, Tue Kjærgaard
Andrei, Adrian Stefan
Lund-Hansen, Lars Chresten
Liu, Yongqin
Hansen, Lars Hestbjerg
author_facet Zeng, Yonghui
Chen, Xihan
Madsen, Anne Mette
Zervas, Athanasios
Nielsen, Tue Kjærgaard
Andrei, Adrian Stefan
Lund-Hansen, Lars Chresten
Liu, Yongqin
Hansen, Lars Hestbjerg
author_sort Zeng, Yonghui
title Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier
title_short Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier
title_full Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier
title_fullStr Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier
title_full_unstemmed Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier
title_sort potential rhodopsin- and bacteriochlorophyll-based dual phototrophy in a high arctic glacier
publishDate 2020
url https://pure.au.dk/portal/da/publications/potential-rhodopsin-and-bacteriochlorophyllbased-dual-phototrophy-in-a-high-arctic-glacier(9b4adc0f-7a32-46b1-af0f-33e37ed2d7fa).html
https://doi.org/10.1128/mBio.02641-20
http://www.scopus.com/inward/record.url?scp=85096815869&partnerID=8YFLogxK
geographic Arctic
Greenland
geographic_facet Arctic
Greenland
genre Arctic
Arctic
glacier
Greenland
genre_facet Arctic
Arctic
glacier
Greenland
op_source Zeng , Y , Chen , X , Madsen , A M , Zervas , A , Nielsen , T K , Andrei , A S , Lund-Hansen , L C , Liu , Y & Hansen , L H 2020 , ' Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier ' , mBio , vol. 11 , no. 6 , e02641-20 , pp. 1-8 . https://doi.org/10.1128/mBio.02641-20
op_relation https://pure.au.dk/portal/da/publications/potential-rhodopsin-and-bacteriochlorophyllbased-dual-phototrophy-in-a-high-arctic-glacier(9b4adc0f-7a32-46b1-af0f-33e37ed2d7fa).html
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