Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia

Abstract Recent studies have identified a significant number of endogenous cellulase genes in various arthropods, including isopods, allowing them to process hydrocarbons efficiently as a food source. While this research has provided insight into underlying gene‐level processes in cellulose decompos...

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Main Authors: Mohammad Javidkar, Steven J. B. Cooper, Nahid Shokri Bousjein, William F. Humphreys, Rachael A. King, Andrew D. Austin
Format: Article
Language:English
Published: Wiley 2023-10-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.10552
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author Mohammad Javidkar
Steven J. B. Cooper
Nahid Shokri Bousjein
William F. Humphreys
Rachael A. King
Andrew D. Austin
author_facet Mohammad Javidkar
Steven J. B. Cooper
Nahid Shokri Bousjein
William F. Humphreys
Rachael A. King
Andrew D. Austin
author_sort Mohammad Javidkar
collection DOAJ
description Abstract Recent studies have identified a significant number of endogenous cellulase genes in various arthropods, including isopods, allowing them to process hydrocarbons efficiently as a food source. While this research has provided insight into underlying gene‐level processes in cellulose decomposition by arthropods, little is known about the existence and expression of cellulase genes in species from cave environments where carbohydrates are sparse. To investigate whether endogenous cellulase genes are maintained in subterranean species, we sequenced the transcriptomes of two subterranean paraplatyarthrid isopod species from calcrete (carbonate) aquifers of central Western Australia and a related surface isopod species. Seven protein‐coding open‐reading frames associated with endoglucanase genes were identified in all species. Orthology inference analyses, using a wide range of cellulase sequences from available databases, supported the endogenous origin of the putative endoglucanase genes. Selection analyses revealed that these genes are primarily subject to purifying selection in most of the sites for both surface and subterranean isopod species, indicating that they are likely to encode functional peptides. Furthermore, evolutionary branch models supported the hypothesis of an adaptive shift in selective pressure acting on the subterranean lineages compared with the ancestral lineage and surface species. Branch‐site models also revealed a few amino acid sites on the subterranean branches to be under positive selection, suggesting the acquisition of novel adaptations to the subterranean environments. These findings also imply that hydrocarbons exist in subsurface aquifers, albeit at reduced levels, and have been utilized by subterranean isopods as a source of energy for millions of years.
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spelling doaj.art-baf2adb8f8a045bb911aba65264009992023-10-27T04:40:51ZengWileyEcology and Evolution2045-77582023-10-011310n/an/a10.1002/ece3.10552Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western AustraliaMohammad Javidkar0Steven J. B. Cooper1Nahid Shokri Bousjein2William F. Humphreys3Rachael A. King4Andrew D. Austin5Department of Ecology and Evolutionary Biology, School of Biological Sciences, and The Environment Institute University of Adelaide Adelaide South Australia AustraliaDepartment of Ecology and Evolutionary Biology, School of Biological Sciences, and The Environment Institute University of Adelaide Adelaide South Australia AustraliaFaculty of Biological Sciences Flinders University Bedford Park South Australia AustraliaWestern Australian Museum Welshpool Western Australia AustraliaDepartment of Ecology and Evolutionary Biology, School of Biological Sciences, and The Environment Institute University of Adelaide Adelaide South Australia AustraliaDepartment of Ecology and Evolutionary Biology, School of Biological Sciences, and The Environment Institute University of Adelaide Adelaide South Australia AustraliaAbstract Recent studies have identified a significant number of endogenous cellulase genes in various arthropods, including isopods, allowing them to process hydrocarbons efficiently as a food source. While this research has provided insight into underlying gene‐level processes in cellulose decomposition by arthropods, little is known about the existence and expression of cellulase genes in species from cave environments where carbohydrates are sparse. To investigate whether endogenous cellulase genes are maintained in subterranean species, we sequenced the transcriptomes of two subterranean paraplatyarthrid isopod species from calcrete (carbonate) aquifers of central Western Australia and a related surface isopod species. Seven protein‐coding open‐reading frames associated with endoglucanase genes were identified in all species. Orthology inference analyses, using a wide range of cellulase sequences from available databases, supported the endogenous origin of the putative endoglucanase genes. Selection analyses revealed that these genes are primarily subject to purifying selection in most of the sites for both surface and subterranean isopod species, indicating that they are likely to encode functional peptides. Furthermore, evolutionary branch models supported the hypothesis of an adaptive shift in selective pressure acting on the subterranean lineages compared with the ancestral lineage and surface species. Branch‐site models also revealed a few amino acid sites on the subterranean branches to be under positive selection, suggesting the acquisition of novel adaptations to the subterranean environments. These findings also imply that hydrocarbons exist in subsurface aquifers, albeit at reduced levels, and have been utilized by subterranean isopods as a source of energy for millions of years.https://doi.org/10.1002/ece3.10552calcrete aquiferscarbohydrateslignocelluloseoniscidea
spellingShingle Mohammad Javidkar
Steven J. B. Cooper
Nahid Shokri Bousjein
William F. Humphreys
Rachael A. King
Andrew D. Austin
Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia
Ecology and Evolution
calcrete aquifers
carbohydrates
lignocellulose
oniscidea
title Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia
title_full Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia
title_fullStr Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia
title_full_unstemmed Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia
title_short Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia
title_sort evolution of endoglucanase genes in subterranean and surface isopod crustaceans from central western australia
topic calcrete aquifers
carbohydrates
lignocellulose
oniscidea
url https://doi.org/10.1002/ece3.10552
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