Genome-wide signals of positive selection in strongylocentrotid sea urchins

Kober, Kord M.; Pogson, Grant H.

doi:10.1186/s12864-017-3944-7

Cited by 15 publications

(28 citation statements)

References 102 publications

(146 reference statements)

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“…We have shown that over deep evolutionary timescales, CCTα displays recurrent signatures of accelerated evolution and structural adaptation in transition from shallow- to deep-sea habitats in brittle stars. This contrasts with previous findings on sea urchins where, CCTε—but not the other subunits—showed signatures of positive section, yet not in the two deep-sea species included in the work ( Kober and Pogson 2017 ). A functional equivalent of the eukaryotic chaperonin CCT in bacteria is the chaperonin complex GroEL/GroES ( Gupta 1990 ; Mayhew et al.…”

Section: Discussioncontrasting

confidence: 99%

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Convergent Evolution and Structural Adaptation to the Deep Ocean in the Protein-Folding Chaperonin CCTα

Weber

Hugall

O’Hara

2020

Genome Biology and Evolution

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The deep ocean is the largest biome on Earth and yet it is among the least studied environments of our planet. Life at great depths requires several specific adaptations, however their molecular mechanisms remain understudied. We examined patterns of positive selection in 416 genes from four brittle star (Ophiuroidea) families displaying replicated events of deep-sea colonization (288 individuals from 216 species). We found consistent signatures of molecular convergence in functions related to protein biogenesis, including protein folding and translation. Five genes were recurrently positively selected, including CCTα (Chaperonin Containing TCP-1 subunit α), which is essential for protein folding. Molecular convergence was detected at the functional and gene levels but not at the amino-acid level. Pressure-adapted proteins are expected to display higher stability to counteract the effects of denaturation. We thus examined in silico local protein stability of CCTα across the ophiuroid tree of life (967 individuals from 725 species) in a phylogenetically-corrected context and found that deep sea-adapted proteins display higher stability within and next to the substrate-binding region, which was confirmed by in silico global protein stability analyses. This suggests that CCTα not only displays structural but also functional adaptations to deep water conditions. The CCT complex is involved in the folding of ∼10% of newly synthesized proteins and has previously been categorized as ‘cold-shock’ protein in numerous eukaryotes. We thus propose that adaptation mechanisms to cold and deep-sea environments may be linked and highlight that efficient protein biogenesis, including protein folding and translation, are key metabolic deep-sea adaptations.

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Section: Discussioncontrasting

confidence: 99%

“…Patterns of positive selection have been investigated to uncover genes underlying adaptation to specific environments, including the deep sea, in nonmodel species ( Oliver et al. 2010 ; Kober and Pogson 2017 ; Sun et al. 2017 ; Weber et al.…”

Section: Introductionmentioning

confidence: 99%

Convergent Evolution and Structural Adaptation to the Deep Ocean in the Protein-Folding Chaperonin CCTα

Weber

Hugall

O’Hara

2020

Genome Biology and Evolution

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“…2005 ; Kosiol et al . 2008 ; Kober and Pogson 2017 ), and suggests limited power to detect positive selection in M. galloprovincialis and M. edulis ( fig. 1 ) within this data.…”

Section: Resultsmentioning

confidence: 99%

“…A consensus alignment for each species was generated for each gene following the methods described in Kober and Pogson (2017) . Unless specified, we performed data processing using BioPerl ( Stajich etal.…”

Section: Methodsmentioning

confidence: 99%

Sequence-Based Analysis of Thermal Adaptation and Protein Energy Landscapes in an Invasive Blue Mussel (Mytilus galloprovincialis)

Saarman

Kober

Simison

et al. 2017

Genome Biology and Evolution

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Adaptive responses to thermal stress in poikilotherms plays an important role in determining competitive ability and species distributions. Amino acid substitutions that affect protein stability and modify the thermal optima of orthologous proteins may be particularly important in this context. Here, we examine a set of 2,770 protein-coding genes to determine if proteins in a highly invasive heat tolerant blue mussel (Mytilus galloprovincialis) contain signals of adaptive increases in protein stability relative to orthologs in a more cold tolerant M. trossulus. Such thermal adaptations might help to explain, mechanistically, the success with which the invasive marine mussel M. galloprovincialis has displaced native species in contact zones in the eastern (California) and western (Japan) Pacific. We tested for stabilizing amino acid substitutions in warm tolerant M. galloprovincialis relative to cold tolerant M. trossulus with a generalized linear model that compares in silico estimates of recent changes in protein stability among closely related congeners. Fixed substitutions in M. galloprovincialis were 3,180.0 calories per mol per substitution more stabilizing at genes with both elevated dN/dS ratios and transcriptional responses to heat stress, and 705.8 calories per mol per substitution more stabilizing across all 2,770 loci investigated. Amino acid substitutions concentrated in a small number of genes were more stabilizing in M. galloprovincialis compared with cold tolerant M. trossulus. We also tested for, but did not find, enrichment of a priori GO terms in genes with elevated dN/dS ratios in M. galloprovincialis. This might indicate that selection for thermodynamic stability is generic across all lineages, and suggests that the high change in estimated protein stability that we observed in M. galloprovincialis is driven by selection for extra stabilizing substitutions, rather than by higher incidence of selection in a greater number of genes in this lineage. Nonetheless, our finding of more stabilizing amino acid changes in the warm adapted lineage is important because it suggests that adaption for thermal stability has contributed to M. galloprovincialis’ superior tolerance to heat stress, and that pairing tests for positive selection and tests for transcriptional response to heat stress can identify candidates of protein stability adaptation.

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“…The Sea Urchin Genome Project has also assembled genome sequences from two additional sea urchins, a sea star, sea cucumber, and brittle star ( ). Four high-quality and three less complete genome assemblies, as well as high coverage, unassembled whole genome sequencing reads are available from other echinoderm species ( 35 – 38 ). In total, the NCBI Short Read Archive hosts 206 projects in 75 echinoderm species that cover all five classes as of this writing.…”

Section: A Wealth Of Echinoderm Genomic Resources Is Availablementioning

confidence: 99%

An Organismal Model for Gene Regulatory Networks in the Gut-Associated Immune Response

Buckley

Rast

2017

Front. Immunol.

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The gut epithelium is an ancient site of complex communication between the animal immune system and the microbial world. While elements of self-non-self receptors and effector mechanisms differ greatly among animal phyla, some aspects of recognition, regulation, and response are broadly conserved. A gene regulatory network (GRN) approach provides a means to investigate the nature of this conservation and divergence even as more peripheral functional details remain incompletely understood. The sea urchin embryo is an unparalleled experimental model for detangling the GRNs that govern embryonic development. By applying this theoretical framework to the free swimming, feeding larval stage of the purple sea urchin, it is possible to delineate the conserved regulatory circuitry that regulates the gut-associated immune response. This model provides a morphologically simple system in which to efficiently unravel regulatory connections that are phylogenetically relevant to immunity in vertebrates. Here, we review the organism-wide cellular and transcriptional immune response of the sea urchin larva. A large set of transcription factors and signal systems, including epithelial expression of interleukin 17 (IL17), are important mediators in the activation of the early gut-associated response. Many of these have homologs that are active in vertebrate immunity, while others are ancient in animals but absent in vertebrates or specific to echinoderms. This larval model provides a means to experimentally characterize immune function encoded in the sea urchin genome and the regulatory interconnections that control immune response and resolution across the tissues of the organism.

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Genome-wide signals of positive selection in strongylocentrotid sea urchins

Cited by 15 publications

References 102 publications

Convergent Evolution and Structural Adaptation to the Deep Ocean in the Protein-Folding Chaperonin CCTα

Convergent Evolution and Structural Adaptation to the Deep Ocean in the Protein-Folding Chaperonin CCTα

Sequence-Based Analysis of Thermal Adaptation and Protein Energy Landscapes in an Invasive Blue Mussel (Mytilus galloprovincialis)

An Organismal Model for Gene Regulatory Networks in the Gut-Associated Immune Response

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