The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation

Abstract The macronuclear (MAC) genomes of ciliates belonging to the genus Euplotes species are comprised of numerous small DNA molecules, nanochromosomes, each typically encoding a single gene. These genomes are responsible for all gene expression during vegetative cell growth. Here, we report the...

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Published in:Scientific Reports
Main Authors: Matteo Mozzicafreddo, Sandra Pucciarelli, Estienne C. Swart, Angela Piersanti, Christiane Emmerich, Giovanna Migliorelli, Patrizia Ballarini, Cristina Miceli
Format: Article in Journal/Newspaper
Language:English
Published: Nature Portfolio 2021
Subjects:
Online Access:https://doi.org/10.1038/s41598-021-98168-5
https://doaj.org/article/ec46624f6a634bca9bb47fdf4d802d4c
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author Matteo Mozzicafreddo
Sandra Pucciarelli
Estienne C. Swart
Angela Piersanti
Christiane Emmerich
Giovanna Migliorelli
Patrizia Ballarini
Cristina Miceli
author_facet Matteo Mozzicafreddo
Sandra Pucciarelli
Estienne C. Swart
Angela Piersanti
Christiane Emmerich
Giovanna Migliorelli
Patrizia Ballarini
Cristina Miceli
author_sort Matteo Mozzicafreddo
collection Directory of Open Access Journals: DOAJ Articles
container_issue 1
container_title Scientific Reports
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description Abstract The macronuclear (MAC) genomes of ciliates belonging to the genus Euplotes species are comprised of numerous small DNA molecules, nanochromosomes, each typically encoding a single gene. These genomes are responsible for all gene expression during vegetative cell growth. Here, we report the analysis of the MAC genome from the Antarctic psychrophile Euplotes focardii. Nanochromosomes containing bacterial sequences were not found, suggesting that phenomena of horizontal gene transfer did not occur recently, even though this ciliate species has a substantial associated bacterial consortium. As in other euplotid species, E. focardii MAC genes are characterized by a high frequency of translational frameshifting. Furthermore, in order to characterize differences that may be consequent to cold adaptation and defense to oxidative stress, the main constraints of the Antarctic marine microorganisms, we compared E. focardii MAC genome with those available from mesophilic Euplotes species. We focussed mainly on the comparison of tubulin, antioxidant enzymes and heat shock protein (HSP) 70 families, molecules which possess peculiar characteristic correlated with cold adaptation in E. focardii. We found that α-tubulin genes and those encoding SODs and CATs antioxidant enzymes are more numerous than in the mesophilic Euplotes species. Furthermore, the phylogenetic trees showed that these molecules are divergent in the Antarctic species. In contrast, there are fewer hsp70 genes in E. focardii compared to mesophilic Euplotes and these genes do not respond to thermal stress but only to oxidative stress. Our results suggest that molecular adaptation to cold and oxidative stress in the Antarctic environment may not only be due to particular amino acid substitutions but also due to duplication and divergence of paralogous genes.
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geographic Antarctic
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spelling ftdoajarticles:oai:doaj.org/article:ec46624f6a634bca9bb47fdf4d802d4c 2025-01-16T19:27:01+00:00 The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation Matteo Mozzicafreddo Sandra Pucciarelli Estienne C. Swart Angela Piersanti Christiane Emmerich Giovanna Migliorelli Patrizia Ballarini Cristina Miceli 2021-09-01T00:00:00Z https://doi.org/10.1038/s41598-021-98168-5 https://doaj.org/article/ec46624f6a634bca9bb47fdf4d802d4c EN eng Nature Portfolio https://doi.org/10.1038/s41598-021-98168-5 https://doaj.org/toc/2045-2322 doi:10.1038/s41598-021-98168-5 2045-2322 https://doaj.org/article/ec46624f6a634bca9bb47fdf4d802d4c Scientific Reports, Vol 11, Iss 1, Pp 1-20 (2021) Medicine R Science Q article 2021 ftdoajarticles https://doi.org/10.1038/s41598-021-98168-5 2022-12-31T05:21:25Z Abstract The macronuclear (MAC) genomes of ciliates belonging to the genus Euplotes species are comprised of numerous small DNA molecules, nanochromosomes, each typically encoding a single gene. These genomes are responsible for all gene expression during vegetative cell growth. Here, we report the analysis of the MAC genome from the Antarctic psychrophile Euplotes focardii. Nanochromosomes containing bacterial sequences were not found, suggesting that phenomena of horizontal gene transfer did not occur recently, even though this ciliate species has a substantial associated bacterial consortium. As in other euplotid species, E. focardii MAC genes are characterized by a high frequency of translational frameshifting. Furthermore, in order to characterize differences that may be consequent to cold adaptation and defense to oxidative stress, the main constraints of the Antarctic marine microorganisms, we compared E. focardii MAC genome with those available from mesophilic Euplotes species. We focussed mainly on the comparison of tubulin, antioxidant enzymes and heat shock protein (HSP) 70 families, molecules which possess peculiar characteristic correlated with cold adaptation in E. focardii. We found that α-tubulin genes and those encoding SODs and CATs antioxidant enzymes are more numerous than in the mesophilic Euplotes species. Furthermore, the phylogenetic trees showed that these molecules are divergent in the Antarctic species. In contrast, there are fewer hsp70 genes in E. focardii compared to mesophilic Euplotes and these genes do not respond to thermal stress but only to oxidative stress. Our results suggest that molecular adaptation to cold and oxidative stress in the Antarctic environment may not only be due to particular amino acid substitutions but also due to duplication and divergence of paralogous genes. Article in Journal/Newspaper Antarc* Antarctic Directory of Open Access Journals: DOAJ Articles Antarctic The Antarctic Scientific Reports 11 1
spellingShingle Medicine
R
Science
Q
Matteo Mozzicafreddo
Sandra Pucciarelli
Estienne C. Swart
Angela Piersanti
Christiane Emmerich
Giovanna Migliorelli
Patrizia Ballarini
Cristina Miceli
The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation
title The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation
title_full The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation
title_fullStr The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation
title_full_unstemmed The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation
title_short The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation
title_sort macronuclear genome of the antarctic psychrophilic marine ciliate euplotes focardii reveals new insights on molecular cold adaptation
topic Medicine
R
Science
Q
topic_facet Medicine
R
Science
Q
url https://doi.org/10.1038/s41598-021-98168-5
https://doaj.org/article/ec46624f6a634bca9bb47fdf4d802d4c