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Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin

Microbial rhodopsin is a simple solar energy-capturing molecule compared to the complex photosynthesis apparatus. Light-driven proton pumping across the cell membrane is a crucial mechanism underlying microbial energy production. Actinobacteria is one of the highly abundant bacterial phyla in freshw...

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Autores principales: Chuon, Kimleng, Kim, So Young, Meas, Seanghun, Shim, Jin-gon, Cho, Shin-Gyu, Kang, Kun-Wook, Kim, Ji-Hyun, Cho, Hyun-Suk, Jung, Kwang-Hwan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8113403/
https://www.ncbi.nlm.nih.gov/pubmed/33995310
http://dx.doi.org/10.3389/fmicb.2021.652328
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author Chuon, Kimleng
Kim, So Young
Meas, Seanghun
Shim, Jin-gon
Cho, Shin-Gyu
Kang, Kun-Wook
Kim, Ji-Hyun
Cho, Hyun-Suk
Jung, Kwang-Hwan
author_facet Chuon, Kimleng
Kim, So Young
Meas, Seanghun
Shim, Jin-gon
Cho, Shin-Gyu
Kang, Kun-Wook
Kim, Ji-Hyun
Cho, Hyun-Suk
Jung, Kwang-Hwan
author_sort Chuon, Kimleng
collection PubMed
description Microbial rhodopsin is a simple solar energy-capturing molecule compared to the complex photosynthesis apparatus. Light-driven proton pumping across the cell membrane is a crucial mechanism underlying microbial energy production. Actinobacteria is one of the highly abundant bacterial phyla in freshwater habitats, and members of this lineage are considered to boost heterotrophic growth via phototrophy, as indicated by the presence of actino-opsin (ActR) genes in their genome. However, it is difficult to validate their function under laboratory settings because Actinobacteria are not consistently cultivable. Based on the published genome sequence of Candidatus aquiluna sp. strain IMCC13023, actinorhodopsin from the strain (ActR-13023) was isolated and characterized in this study. Notably, ActR-13023 assembled with natively synthesized carotenoid/retinal (used as a dual chromophore) and functioned as a light-driven outward proton pump. The ActR-13023 gene and putative genes involved in the chromophore (retinal/carotenoid) biosynthetic pathway were detected in the genome, indicating the functional expression ActR-13023 under natural conditions for the utilization of solar energy for proton translocation. Heterologous expressed ActR-13023 exhibited maximum absorption at 565 nm with practical proton pumping ability. Purified ActR-13023 could be reconstituted with actinobacterial carotenoids for additional light-harvesting. The existence of actinorhodopsin and its chromophore synthesis machinery in Actinobacteria indicates the inherent photo-energy conversion function of this microorganism. The assembly of ActR-13023 to its synthesized chromophores validated the microbial community’s importance in the energy cycle.
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spelling pubmed-81134032021-05-13 Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin Chuon, Kimleng Kim, So Young Meas, Seanghun Shim, Jin-gon Cho, Shin-Gyu Kang, Kun-Wook Kim, Ji-Hyun Cho, Hyun-Suk Jung, Kwang-Hwan Front Microbiol Microbiology Microbial rhodopsin is a simple solar energy-capturing molecule compared to the complex photosynthesis apparatus. Light-driven proton pumping across the cell membrane is a crucial mechanism underlying microbial energy production. Actinobacteria is one of the highly abundant bacterial phyla in freshwater habitats, and members of this lineage are considered to boost heterotrophic growth via phototrophy, as indicated by the presence of actino-opsin (ActR) genes in their genome. However, it is difficult to validate their function under laboratory settings because Actinobacteria are not consistently cultivable. Based on the published genome sequence of Candidatus aquiluna sp. strain IMCC13023, actinorhodopsin from the strain (ActR-13023) was isolated and characterized in this study. Notably, ActR-13023 assembled with natively synthesized carotenoid/retinal (used as a dual chromophore) and functioned as a light-driven outward proton pump. The ActR-13023 gene and putative genes involved in the chromophore (retinal/carotenoid) biosynthetic pathway were detected in the genome, indicating the functional expression ActR-13023 under natural conditions for the utilization of solar energy for proton translocation. Heterologous expressed ActR-13023 exhibited maximum absorption at 565 nm with practical proton pumping ability. Purified ActR-13023 could be reconstituted with actinobacterial carotenoids for additional light-harvesting. The existence of actinorhodopsin and its chromophore synthesis machinery in Actinobacteria indicates the inherent photo-energy conversion function of this microorganism. The assembly of ActR-13023 to its synthesized chromophores validated the microbial community’s importance in the energy cycle. Frontiers Media S.A. 2021-04-28 /pmc/articles/PMC8113403/ /pubmed/33995310 http://dx.doi.org/10.3389/fmicb.2021.652328 Text en Copyright © 2021 Chuon, Kim, Meas, Shim, Cho, Kang, Kim, Cho and Jung. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Chuon, Kimleng
Kim, So Young
Meas, Seanghun
Shim, Jin-gon
Cho, Shin-Gyu
Kang, Kun-Wook
Kim, Ji-Hyun
Cho, Hyun-Suk
Jung, Kwang-Hwan
Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin
title Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin
title_full Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin
title_fullStr Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin
title_full_unstemmed Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin
title_short Assembly of Natively Synthesized Dual Chromophores Into Functional Actinorhodopsin
title_sort assembly of natively synthesized dual chromophores into functional actinorhodopsin
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8113403/
https://www.ncbi.nlm.nih.gov/pubmed/33995310
http://dx.doi.org/10.3389/fmicb.2021.652328
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