Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>

The archaeon <i>Cuniculiplasma divulgatum</i> is ubiquitous in acidic environments with low-to-moderate temperatures. However, molecular mechanisms underlying its ability to thrive at lower temperatures remain unexplored. Using mass spectrometry (MS)-based proteomics, we analysed the eff...

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Main Authors: Rafael Bargiela, Karin Lanthaler, Colin M. Potter, Manuel Ferrer, Alexander F. Yakunin, Bela Paizs, Peter N. Golyshin, Olga V. Golyshina
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/5/759
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author Rafael Bargiela
Karin Lanthaler
Colin M. Potter
Manuel Ferrer
Alexander F. Yakunin
Bela Paizs
Peter N. Golyshin
Olga V. Golyshina
author_facet Rafael Bargiela
Karin Lanthaler
Colin M. Potter
Manuel Ferrer
Alexander F. Yakunin
Bela Paizs
Peter N. Golyshin
Olga V. Golyshina
author_sort Rafael Bargiela
collection DOAJ
description The archaeon <i>Cuniculiplasma divulgatum</i> is ubiquitous in acidic environments with low-to-moderate temperatures. However, molecular mechanisms underlying its ability to thrive at lower temperatures remain unexplored. Using mass spectrometry (MS)-based proteomics, we analysed the effect of short-term (3 h) exposure to cold. The <i>C. divulgatum</i> genome encodes 2016 protein-coding genes, from which 819 proteins were identified in the cells grown under optimal conditions. In line with the peptidolytic lifestyle of <i>C. divulgatum</i>, its intracellular proteome revealed the abundance of proteases, ABC transporters and cytochrome C oxidase. From 747 quantifiable polypeptides, the levels of 582 proteins showed no change after the cold shock, whereas 104 proteins were upregulated suggesting that they might be contributing to cold adaptation. The highest increase in expression appeared in low-abundance (0.001–0.005 fmol%) proteins for polypeptides’ hydrolysis (metal-dependent hydrolase), oxidation of amino acids (FAD-dependent oxidoreductase), pyrimidine biosynthesis (aspartate carbamoyltransferase regulatory chain proteins), citrate cycle (2-oxoacid ferredoxin oxidoreductase) and ATP production (V type ATP synthase). Importantly, the cold shock induced a substantial increase (6% and 9%) in expression of the most-abundant proteins, thermosome beta subunit and glutamate dehydrogenase. This study has outlined potential mechanisms of environmental fitness of <i>Cuniculiplasma</i> spp. allowing them to colonise acidic settings at low/moderate temperatures.
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spelling doaj.art-ae9e1a4e4b08496bbe5f5e17a5be0d992023-11-20T00:55:53ZengMDPI AGMicroorganisms2076-26072020-05-018575910.3390/microorganisms8050759Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>Rafael Bargiela0Karin Lanthaler1Colin M. Potter2Manuel Ferrer3Alexander F. Yakunin4Bela Paizs5Peter N. Golyshin6Olga V. Golyshina7School of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKSchool of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKSchool of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKSystems Biotechnology Group, Department of Applied Biocatalysis, CSIC—Institute of Catalysis, Marie Curie 2, 28049 Madrid, SpainSchool of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKSchool of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKSchool of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKSchool of Natural Sciences, Bangor University, Deiniol Rd, Bangor LL57 2UW, UKThe archaeon <i>Cuniculiplasma divulgatum</i> is ubiquitous in acidic environments with low-to-moderate temperatures. However, molecular mechanisms underlying its ability to thrive at lower temperatures remain unexplored. Using mass spectrometry (MS)-based proteomics, we analysed the effect of short-term (3 h) exposure to cold. The <i>C. divulgatum</i> genome encodes 2016 protein-coding genes, from which 819 proteins were identified in the cells grown under optimal conditions. In line with the peptidolytic lifestyle of <i>C. divulgatum</i>, its intracellular proteome revealed the abundance of proteases, ABC transporters and cytochrome C oxidase. From 747 quantifiable polypeptides, the levels of 582 proteins showed no change after the cold shock, whereas 104 proteins were upregulated suggesting that they might be contributing to cold adaptation. The highest increase in expression appeared in low-abundance (0.001–0.005 fmol%) proteins for polypeptides’ hydrolysis (metal-dependent hydrolase), oxidation of amino acids (FAD-dependent oxidoreductase), pyrimidine biosynthesis (aspartate carbamoyltransferase regulatory chain proteins), citrate cycle (2-oxoacid ferredoxin oxidoreductase) and ATP production (V type ATP synthase). Importantly, the cold shock induced a substantial increase (6% and 9%) in expression of the most-abundant proteins, thermosome beta subunit and glutamate dehydrogenase. This study has outlined potential mechanisms of environmental fitness of <i>Cuniculiplasma</i> spp. allowing them to colonise acidic settings at low/moderate temperatures.https://www.mdpi.com/2076-2607/8/5/759Acidophilic archaeaacidic environmentsacid mine drainage systems<i>Thermoplasmatales</i><i>Cuniculiplasma</i>proteome
spellingShingle Rafael Bargiela
Karin Lanthaler
Colin M. Potter
Manuel Ferrer
Alexander F. Yakunin
Bela Paizs
Peter N. Golyshin
Olga V. Golyshina
Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>
Microorganisms
Acidophilic archaea
acidic environments
acid mine drainage systems
<i>Thermoplasmatales</i>
<i>Cuniculiplasma</i>
proteome
title Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>
title_full Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>
title_fullStr Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>
title_full_unstemmed Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>
title_short Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, <i>Cuniculiplasma divulgatum</i>
title_sort proteome cold shock response in the extremely acidophilic archaeon i cuniculiplasma divulgatum i
topic Acidophilic archaea
acidic environments
acid mine drainage systems
<i>Thermoplasmatales</i>
<i>Cuniculiplasma</i>
proteome
url https://www.mdpi.com/2076-2607/8/5/759
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