The molecular evolutionary dynamics of oxidative phosphorylation (OXPHOS) genes in Hymenoptera

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Abstract

Background

The primary energy-producing pathway in eukaryotic cells, the oxidative phosphorylation (OXPHOS) system, comprises proteins encoded by both mitochondrial and nuclear genes. To maintain the function of the OXPHOS system, the pattern of substitutions in mitochondrial and nuclear genes may not be completely independent. It has been suggested that slightly deleterious substitutions in mitochondrial genes are compensated by substitutions in the interacting nuclear genes due to positive selection. Among the four largest insect orders, Coleoptera (beetles), Hymenoptera (sawflies, wasps, ants, and bees), Diptera (midges, mosquitoes, and flies) and Lepidoptera (moths and butterflies), the mitochondrial genes of Hymenoptera exhibit an exceptionally high amino acid substitution rate while the evolution of nuclear OXPHOS genes is largely unknown. Therefore, Hymenoptera is an excellent model group for testing the hypothesis of positive selection driving the substitution rate of nuclear OXPHOS genes. In this study, we report the evolutionary rate of OXPHOS genes in Hymenoptera and test for evidence of positive selection in nuclear OXPHOS genes of Hymenoptera.

Results

Our analyses revealed that the amino acid substitution rate of mitochondrial and nuclear OXPHOS genes in Hymenoptera is higher than that in other studied insect orders. In contrast, the amino acid substitution rate of non-OXPHOS genes in Hymenoptera is lower than the rate in other insect orders. Overall, we found the dN/ dS ratio of the nuclear OXPHOS genes to be higher in Hymenoptera than in other insect orders. However, nuclear OXPHOS genes with high dN/ dS ratio did not always exhibit a high amino acid substitution rate. Using branch-site and site model tests, we identified various codon sites that evolved under positive selection in nuclear OXPHOS genes.

Conclusions

Our results showed that nuclear OXPHOS genes in Hymenoptera are evolving faster than the genes in other three insect orders. The branch test suggested that while some nuclear OXPHOS genes in Hymenoptera show a signature of positive selection, the pattern is not consistent across all nuclear OXPHOS genes. As only few codon sites were under positive selection, we suggested that positive selection might not be the only factor contributing to the rapid evolution of nuclear OXPHOS genes in Hymenoptera.

Electronic supplementary material

The online version of this article (10.1186/s12862-017-1111-z) contains supplementary material, which is available to authorized users.

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Most cited references 31

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Energy metabolism of cancer: Glycolysis versus oxidative phosphorylation (Review).

Jie Zheng (2012)

Metabolic activities in normal cells rely primarily on mitochondrial oxidative phosphorylation (OXPHOS) to generate ATP for energy. Unlike in normal cells, glycolysis is enhanced and OXPHOS capacity is reduced in various cancer cells. It has long been believed that the glycolytic phenotype in cancer is due to a permanent impairment of mitochondrial OXPHOS, as proposed by Otto Warburg. This view is challenged by recent investigations which find that the function of mitochondrial OXPHOS in most cancers is intact. Aerobic glycolysis in many cancers is the combined result of various factors such as oncogenes, tumor suppressors, a hypoxic microenvironment, mtDNA mutations, genetic background and others. Understanding the features and complexity of the cancer energy metabolism will help to develop new approaches in early diagnosis and effectively target therapy of cancer.

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A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities?

Ronald Burton, Felipe S. Barreto (2012)

Evolution in allopatric populations can lead to incompatibilities that result in reduced hybrid fitness and ultimately reproductive isolation upon secondary contact. The Dobzhansky-Muller (DM) model nicely accounts for the evolution of such incompatibilities. Although DM incompatibilities were originally conceived as resulting of interactions between nuclear genes, recent studies have documented cases where incompatibilities have arisen between nuclear and mitochondrial genomes (mtDNA). Although mtDNA comprises only a tiny component (typically <0.01%) of an organism's genetic material, several features of mtDNA may lead to a disproportionate contribution to the evolution of hybrid incompatibilities: (i) essentially all functions of mtDNA require interaction with nuclear gene products. All mtDNA-encoded proteins are components of the oxidative phosphorylation (OXPHOS) system and all mtDNA-encoded RNAs are part of the mitochondrial protein synthetic machinery; both processes require interaction with nuclear-encoded proteins for function. (ii) Transcription and replication of mtDNA also involve mitonuclear interactions as nuclear-encoded proteins must bind to regulatory motifs in the mtDNA to initiate these processes. (iii) Although features of mtDNA vary amongst taxa, metazoan mtDNA is typically characterized by high nucleotide substitution rates, lack of recombination and reduced effective population sizes that collectively lead to increased chance fixation of mildly deleterious mutations. Combined, these features create an evolutionary dynamic where rapid mtDNA evolution favours compensatory nuclear gene evolution, ultimately leading to co-adaptation of mitochondrial and nuclear genomes. When previously isolated lineages hybridize in nature or in the lab, intergenomic co-adaptation is disrupted and hybrid breakdown is observed; the role of intergenomic co-adaptation in hybrid breakdown and speciation will generally be most pronounced when rates of mtDNA evolution are high or when restricted gene flow results in significant population differentiation. © 2012 Blackwell Publishing Ltd.

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Is Open Access

Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification

Xin Zhou, Yiyuan Li, Shanlin Liu … (2013)

Background Next-generation-sequencing (NGS) technologies combined with a classic DNA barcoding approach have enabled fast and credible measurement for biodiversity of mixed environmental samples. However, the PCR amplification involved in nearly all existing NGS protocols inevitably introduces taxonomic biases. In the present study, we developed new Illumina pipelines without PCR amplifications to analyze terrestrial arthropod communities. Results Mitochondrial enrichment directly followed by Illumina shotgun sequencing, at an ultra-high sequence volume, enabled the recovery of Cytochrome c Oxidase subunit 1 (COI) barcode sequences, which allowed for the estimation of species composition at high fidelity for a terrestrial insect community. With 15.5 Gbp Illumina data, approximately 97% and 92% were detected out of the 37 input Operational Taxonomic Units (OTUs), whether the reference barcode library was used or not, respectively, while only 1 novel OTU was found for the latter. Additionally, relatively strong correlation between the sequencing volume and the total biomass was observed for species from the bulk sample, suggesting a potential solution to reveal relative abundance. Conclusions The ability of the new Illumina PCR-free pipeline for DNA metabarcoding to detect small arthropod specimens and its tendency to avoid most, if not all, false positives suggests its great potential in biodiversity-related surveillance, such as in biomonitoring programs. However, further improvement for mitochondrial enrichment is likely needed for the application of the new pipeline in analyzing arthropod communities at higher diversity.

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Author and article information

Contributors

Yiyuan Li: yli19@nd.edu

Rui Zhang: zhangrui1@genomics.cn

Shanlin Liu: liushanlin@genomics.cn

Alexander Donath: a.donath@leibniz-zfmk.de

Ralph S. Peters: r.peters@leibniz-zfmk.de

Jessica Ware: jware42@newark.rutgers.edu

Bernhard Misof: bmisof@uni-bonn.de

Oliver Niehuis: oliver.niehuis@biologie.uni-freiburg.de

Michael E. Pfrender: Michael.Pfrender.1@nd.edu

Xin Zhou:

ORCID: http://orcid.org/0000-0002-1407-7952

xinzhou@cau.edu.cn

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 28 December 2017

Publication date PMC-release: 28 December 2017

Publication date Collection: 2017

Volume: 17

Electronic Location Identifier: 269

Affiliations

[1 ]ISNI 0000 0001 2168 0066, GRID grid.131063.6, Department of Biological Sciences, , University of Notre Dame, ; Notre Dame, IN USA

[2 ]Environmental Change Initiative, Notre Dame, IN USA

[3 ]ISNI 0000 0001 2034 1839, GRID grid.21155.32, China National GeneBank, BGI-Shenzhen, ; Guangdong Province, Shenzhen, China

[4 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Centre for GeoGenetics, Natural History Museum of Denmark, , University of Copenhagen, ; Copenhagen, Denmark

[5 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Zoologisches Forschungsmuseum Alexander Koenig, Zentrum für Molekulare Biodiversitätsforschung (zmb), ; Bonn, Germany

[6 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Zoologisches Forschungsmuseum Alexander Koenig, Abteilung Arthropoda, ; Bonn, Germany

[7 ]ISNI 0000 0004 1936 8796, GRID grid.430387.b, Department of Biological Sciences, , Rutgers University, ; Newark, NJ 07102 USA

[8 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, ; Bonn, Germany

[9 ]GRID grid.5963.9, Evolutionary Biology and Animal Ecology, Institute of Biology I (Zoology), , Albert Ludwig University of Freiburg, ; Hauptstr. 1, 79104 Freiburg, Germany

[10 ]ISNI 0000 0004 0530 8290, GRID grid.22935.3f, Beijing Advanced Innovation Center for Food Nutrition and Human Health, , China Agricultural University, ; Beijing, 100193 China

[11 ]ISNI 0000 0004 0530 8290, GRID grid.22935.3f, Department of Entomology, , China Agricultural University, ; Beijing, 100193 China

Author information

Xin Zhou http://orcid.org/0000-0002-1407-7952

Article

Publisher ID: 1111

DOI: 10.1186/s12862-017-1111-z

PMC ID: 5745899

PubMed ID: 29281964

SO-VID: 7d5d1ded-a641-402c-bca4-fb3798b2dd6a

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 10 May 2017

Date accepted : 8 December 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100005236, Chinese Universities Scientific Fund;

Award ID: 2017QC114

Award Recipient : Xin Zhou

Custom metadata

ScienceOpen disciplines: Evolutionary Biology

Keywords: molecular evolution,positive selection,mitochondrial-nuclear interaction,insects

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ScienceOpen disciplines: Evolutionary Biology

Keywords: molecular evolution, positive selection, mitochondrial-nuclear interaction, insects

The molecular evolutionary dynamics of oxidative phosphorylation (OXPHOS) genes in Hymenoptera

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Abstract

Background

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Hymenoptera

Most cited references 31

Energy metabolism of cancer: Glycolysis versus oxidative phosphorylation (Review).

A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities?

Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification

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