Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum

Persistent Link:
http://hdl.handle.net/10150/610286
Title:
Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum
Author:
Lasek-Nesselquist, Erica; Wisecaver, Jennifer H.; Hackett, Jeremiah D.; Johnson, Matthew D.
Affiliation:
University of Scranton; Vanderbilt University; University of Arizona; Woods Hole Oceanographic Institution
Issue Date:
2015
Publisher:
BioMed Central Ltd
Citation:
Lasek-Nesselquist et al. BMC Genomics (2015) 16:805 DOI 10.1186/s12864-015-2052-9
Journal:
BMC Genomics
Rights:
© 2015 Lasek-Nesselquist et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/)
Collection Information:
This item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.
Abstract:
BACKGROUND: Organelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids. Mesodinium rubrum is an abundant and broadly distributed photosynthetic marine ciliate that steals organelles from cryptophyte algae, such as Geminigera cryophila. M. rubrum is unique from most other acquired phototrophs because it also steals a functional nucleus that facilitates genetic control of sequestered plastids and other organelles. We analyzed changes in G. cryophila nuclear gene expression and transcript abundance after its incorporation into the cellular architecture of M. rubrum as an initial step towards understanding this complex system. METHODS: We compared Illumina-generated transcriptomes of the cryptophyte Geminigera cryophila as a free-living cell and as a sequestered nucleus in M. rubrum to identify changes in protein abundance and gene expression. After KEGG annotation, proteins were clustered by functional categories, which were evaluated for over- or under-representation in the sequestered nucleus. Similarly, coding sequences were grouped by KEGG categories/ pathways, which were then evaluated for over- or under-expression via read count strategies. RESULTS: At the time of sampling, the global transcriptome of M. rubrum was dominated (~58-62 %) by transcription from its stolen nucleus. A comparison of transcriptomes from free-living G. cryophila cells to those of the sequestered nucleus revealed a decrease in gene expression and transcript abundance for most functional protein categories within the ciliate. However, genes coding for proteins involved in photosynthesis, oxidative stress reduction, and several other metabolic pathways revealed striking exceptions to this general decline. CONCLUSIONS: Major changes in G. cryophila transcript expression after sequestration by M. rubrum and the ciliate's success as a photoautotroph imply some level of control or gene regulation by the ciliate and at the very least reflect a degree of coordination between host and foreign organelles. Intriguingly, cryptophyte genes involved in protein transport are significantly under-expressed in M. rubrum, implicating a role for the ciliate's endomembrane system in targeting cryptophyte proteins to plastid complexes. Collectively, this initial portrait of an acquired transcriptome within a dynamic and ecologically successful ciliate highlights the remarkable cellular and metabolic chimerism of this system.
EISSN:
1471-2164
DOI:
10.1186/s12864-015-2052-9
Keywords:
Mesodinium rubrum; Geminigera cryophila; Karyoklepty; Acquired phototrophy; Transcriptome; Differential gene expression; Chimeric metabolism; Organelle retention; Mixotrophy
Version:
Final published version
Additional Links:
http://www.biomedcentral.com/1471-2164/16/805

Full metadata record

DC FieldValue Language
dc.contributor.authorLasek-Nesselquist, Ericaen
dc.contributor.authorWisecaver, Jennifer H.en
dc.contributor.authorHackett, Jeremiah D.en
dc.contributor.authorJohnson, Matthew D.en
dc.date.accessioned2016-05-20T09:03:17Z-
dc.date.available2016-05-20T09:03:17Z-
dc.date.issued2015en
dc.identifier.citationLasek-Nesselquist et al. BMC Genomics (2015) 16:805 DOI 10.1186/s12864-015-2052-9en
dc.identifier.doi10.1186/s12864-015-2052-9en
dc.identifier.urihttp://hdl.handle.net/10150/610286-
dc.description.abstractBACKGROUND: Organelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids. Mesodinium rubrum is an abundant and broadly distributed photosynthetic marine ciliate that steals organelles from cryptophyte algae, such as Geminigera cryophila. M. rubrum is unique from most other acquired phototrophs because it also steals a functional nucleus that facilitates genetic control of sequestered plastids and other organelles. We analyzed changes in G. cryophila nuclear gene expression and transcript abundance after its incorporation into the cellular architecture of M. rubrum as an initial step towards understanding this complex system. METHODS: We compared Illumina-generated transcriptomes of the cryptophyte Geminigera cryophila as a free-living cell and as a sequestered nucleus in M. rubrum to identify changes in protein abundance and gene expression. After KEGG annotation, proteins were clustered by functional categories, which were evaluated for over- or under-representation in the sequestered nucleus. Similarly, coding sequences were grouped by KEGG categories/ pathways, which were then evaluated for over- or under-expression via read count strategies. RESULTS: At the time of sampling, the global transcriptome of M. rubrum was dominated (~58-62 %) by transcription from its stolen nucleus. A comparison of transcriptomes from free-living G. cryophila cells to those of the sequestered nucleus revealed a decrease in gene expression and transcript abundance for most functional protein categories within the ciliate. However, genes coding for proteins involved in photosynthesis, oxidative stress reduction, and several other metabolic pathways revealed striking exceptions to this general decline. CONCLUSIONS: Major changes in G. cryophila transcript expression after sequestration by M. rubrum and the ciliate's success as a photoautotroph imply some level of control or gene regulation by the ciliate and at the very least reflect a degree of coordination between host and foreign organelles. Intriguingly, cryptophyte genes involved in protein transport are significantly under-expressed in M. rubrum, implicating a role for the ciliate's endomembrane system in targeting cryptophyte proteins to plastid complexes. Collectively, this initial portrait of an acquired transcriptome within a dynamic and ecologically successful ciliate highlights the remarkable cellular and metabolic chimerism of this system.en
dc.language.isoenen
dc.publisherBioMed Central Ltden
dc.relation.urlhttp://www.biomedcentral.com/1471-2164/16/805en
dc.rights© 2015 Lasek-Nesselquist et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/)en
dc.subjectMesodinium rubrumen
dc.subjectGeminigera cryophilaen
dc.subjectKaryokleptyen
dc.subjectAcquired phototrophyen
dc.subjectTranscriptomeen
dc.subjectDifferential gene expressionen
dc.subjectChimeric metabolismen
dc.subjectOrganelle retentionen
dc.subjectMixotrophyen
dc.titleInsights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrumen
dc.typeArticleen
dc.identifier.eissn1471-2164en
dc.contributor.departmentUniversity of Scrantonen
dc.contributor.departmentVanderbilt Universityen
dc.contributor.departmentUniversity of Arizonaen
dc.contributor.departmentWoods Hole Oceanographic Institutionen
dc.identifier.journalBMC Genomicsen
dc.description.collectioninformationThis item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
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