The Adaptations of Arthropods to Extreme Environments

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Other Arthropods and General Topics".

Deadline for manuscript submissions: closed (15 April 2022) | Viewed by 22585

Special Issue Editors


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Guest Editor
Molecular Biomimetics Research Unit, Institute of Agrobiological Sciences, National Institute of Agriculture and Food Research Organization (NARO), Tsukuba, Japan
Interests: insect physiology; anhydrobiosis; biotechnologies related to dry storage; adaptations to extreme environments; Chironomid midges
1. KFU-RIKEN Translational Genomics Unit, RIKEN, Yokohama 351-0198, Japan
2. Graduate School of Medicine, Juntendo University, Tokyo 113-8421, Japan
Interests: multi-omics; extremophiles; comparative genomics; high-throughput sequencing technologies

Special Issue Information

Dear Colleagues,

Our planet has a large variety of environments harboring a tremendous biodiversity of organisms adapted to these specific conditions. Stable and propitious environments are rare, and life often has to face extreme variations of the environment, such as freezing winters, heatwaves, drought, floods, etc. Arthropods are widely distributed on Earth and have evolved behavioral, morphological, and especially physiological adaptations to cope with such extreme environmental conditions. Diapause is probably the most investigated adaptation to temporary harsh conditions, but cryptobiosis, which allows survival in even more extreme environments, has also been a focus of tolerance biology for decades. Other adaptations to hypersaline, acidic, hypoxic, or highly hydrostatic conditions, for instance, make invertebrates champions for the colonization of extreme environments.

This Special Issue will report recent discoveries about how arthropods manage to survive the extreme conditions of their environment. In the context of global warming associated with extreme meteorological events, we have still a lot to learn from invertebrates about how to adapt to a harsher environment.

Dr. Richard Cornette
Dr. Oleg Gusev
Guest Editors

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Keywords

  • stress tolerance
  • diapause
  • cryptobiosis
  • desiccation
  • freeze tolerance
  • adaptation
  • arthropods

Published Papers (8 papers)

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Research

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21 pages, 17603 KiB  
Article
Resistance to Extreme Stresses by a Newly Discovered Japanese Tardigrade Species, Macrobiotus kyoukenus (Eutardigrada, Macrobiotidae)
by Michele Cesari, Ilaria Giovannini, Tiziana Altiero, Roberto Guidetti, Richard Cornette, Takahiro Kikawada and Lorena Rebecchi
Insects 2022, 13(7), 634; https://doi.org/10.3390/insects13070634 - 15 Jul 2022
Cited by 9 | Viewed by 2302
Abstract
Tardigrades are small micrometazoans able to resist several environmental stresses in any stage of their life cycle. An integrated analysis of tardigrade specimens collected in Tsukuba (Japan) revealed a peculiar morphology and a new sensory field in the cloaca. Molecular taxonomy and phylogenetic [...] Read more.
Tardigrades are small micrometazoans able to resist several environmental stresses in any stage of their life cycle. An integrated analysis of tardigrade specimens collected in Tsukuba (Japan) revealed a peculiar morphology and a new sensory field in the cloaca. Molecular taxonomy and phylogenetic analysis on different genes (COI, ITS2, 18S and 28S) confirmed that this population is a new species, Macrobiotus kyoukenus sp. nov., belonging to the widespread Macrobiotus hufelandi group. The stress resistance capabilities of M. kyoukenus sp. nov. have been tested by submitting animals to extreme desiccation, rapid freezing, and high levels of ultraviolet radiations (UVB and UVC). Animals were able to survive desiccation (survivorship 95.71 ± 7.07%) and freezing up to −80 °C (82.33 ± 17.11%). Both hydrated and desiccated animals showed a high tolerance to increasing UV radiations: hydrated animals survived to doses up to 152.22 kJ m−2 (UVB) and up to 15.00 kJ m−2 (UVC), while desiccated specimens persisted to radiations up to 165.12 kJ m−2 (UVB) and up to 35.00 kJ m−2 (UVC). Present data contribute to the discovery of a larger tardigrade biodiversity in Japan, and the tolerance capabilities of M. kyoukenus sp. nov. show that it could become a new emerging model for stress resistance studies. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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15 pages, 3349 KiB  
Article
Metabolic Tolerance to Atmospheric Pressure of Two Freshwater Endemic Amphipods Mostly Inhabiting the Deep-Water Zone of the Ancient Lake Baikal
by Ekaterina Madyarova, Yulia Shirokova, Anton Gurkov, Polina Drozdova, Boris Baduev, Yulia Lubyaga, Zhanna Shatilina, Maria Vishnevskaya and Maxim Timofeyev
Insects 2022, 13(7), 578; https://doi.org/10.3390/insects13070578 - 24 Jun 2022
Viewed by 1882
Abstract
Lake Baikal is the only freshwater reservoir inhabited by deep-water fauna, which originated mostly from shallow-water ancestors. Ommatogammarus flavus and O. albinus are endemic scavenger amphipods (Amphipoda, Crustacea) dwelling in wide depth ranges of the lake covering over 1300 m. O. flavus had [...] Read more.
Lake Baikal is the only freshwater reservoir inhabited by deep-water fauna, which originated mostly from shallow-water ancestors. Ommatogammarus flavus and O. albinus are endemic scavenger amphipods (Amphipoda, Crustacea) dwelling in wide depth ranges of the lake covering over 1300 m. O. flavus had been previously collected close to the surface, while O. albinus has never been found above the depth of 47 m. Since O. albinus is a promising model species for various research, here we tested whether O. albinus is less metabolically adapted to atmospheric pressure than O. flavus. We analyzed a number of energy-related traits (contents of glucose, glycogen and adenylates, as well as lactate dehydrogenase activity) and oxidative stress markers (activities of antioxidant enzymes and levels of lipid peroxidation products) after sampling from different depths and after both species’ acclimation to atmospheric pressure. The analyses were repeated in two independent sampling campaigns. We found no consistent signs of metabolic disturbances or oxidative stress in both species right after lifting. Despite O. flavus surviving slightly better in laboratory conditions, during long-term acclimation, both species showed comparable reactions without critical changes. Thus, the obtained data favor using O. albinus along with O. flavus for physiological research under laboratory conditions. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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13 pages, 7874 KiB  
Article
Identification and Characterization of Antioxidant Enzyme Genes in Parasitoid Aphelinus asychis (Hymenoptera: Aphelinidae) and Expression Profiling Analysis under Temperature Stress
by Xiang Liu, Zhi-Xiao Fu, Zhi-Wei Kang, Hao Li, Tong-Xian Liu and Dun Wang
Insects 2022, 13(5), 447; https://doi.org/10.3390/insects13050447 - 09 May 2022
Cited by 4 | Viewed by 1893
Abstract
It is well known that high temperature, a typically negative environmental factor, reduces the parasitism of a parasitoid. Generally, high temperature causes the rapid overproduction of reactive oxygen species (ROS) in organisms, and antioxidative enzymes participate in the process of resisting environmental stress [...] Read more.
It is well known that high temperature, a typically negative environmental factor, reduces the parasitism of a parasitoid. Generally, high temperature causes the rapid overproduction of reactive oxygen species (ROS) in organisms, and antioxidative enzymes participate in the process of resisting environmental stress by eliminating excess ROS. In the present study, we identify two superoxide dismutase (SOD), one catalase (CAT), six peroxidases (POD), and five glutathione-S-transferase (GST) genes; and the survival rate and antioxidative enzyme patterns under short-term high temperature exposure of the parasitoid wasp, A.asychis, are examined. Survival results of A.asychis reveal that females show higher thermal tolerance than males. Under short-term high-temperature exposure, in females, the expression levels of most antioxidant enzyme genes decreased first and then increased to a peak at 41 °C, while only the expression of AasyGST4 showed a continuous increase. In males, the expression patterns of most antioxidant enzyme genes fluctuated and reached a maximum at 41 °C. Moreover, the expression levels of the majority of antioxidant enzyme genes were higher in females than in males. In addition, at temperatures of and above 35 °C, the activities of these four antioxidant enzymes were induced. The results show that the antioxidant enzymes confer thermo-tolerance to A. asychis against lethal thermal stress. Our observations enrich the understanding of the response mechanism to high-temperature assaults of A. asychis. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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14 pages, 110421 KiB  
Article
Development of a Tet-On Inducible Expression System for the Anhydrobiotic Cell Line, Pv11
by Shoko Tokumoto, Yugo Miyata, Kengo Usui, Ruslan Deviatiiarov, Takahiro Ohkawa, Sabina Kondratieva, Elena Shagimardanova, Oleg Gusev, Richard Cornette, Masayoshi Itoh, Yoshihide Hayashizaki and Takahiro Kikawada
Insects 2020, 11(11), 781; https://doi.org/10.3390/insects11110781 - 11 Nov 2020
Cited by 5 | Viewed by 3163
Abstract
The Pv11 cell line established from an African chironomid, Polypedilum vanderplanki, is the only cell line tolerant to complete desiccation. In Pv11 cells, a constitutive expression system for Pv11 cells was previously exploited and several reporter genes were successfully expressed. Here we [...] Read more.
The Pv11 cell line established from an African chironomid, Polypedilum vanderplanki, is the only cell line tolerant to complete desiccation. In Pv11 cells, a constitutive expression system for Pv11 cells was previously exploited and several reporter genes were successfully expressed. Here we report the identification of an effective minimal promoter for Pv11 cells and its application to the Tet-On inducible expression system. First, using a luciferase reporter assay, we showed that a 202 bp deletion fragment derived from the constitutively active 121-promoter functions in Pv11 cells as an appropriate minimal promoter with the Tet-On inducible expression system. The AcGFP1 (Aequorea coerulescens green fluorescent protein) was also successfully expressed in Pv11 cells using the inducible system. In addition to these reporter genes, the avian myeloblastosis virus reverse transcriptase α subunit (AMV RTα), which is one of the most widely commercially available RNA-dependent DNA polymerases, was successfully expressed through the inducible expression system and its catalytic activity was verified. These results demonstrate the establishment of an inducible expression system in cells that can be preserved in the dry state and highlight a possible application to the production of large and complex proteins. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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11 pages, 1595 KiB  
Article
Diversity and Regulation of S-Adenosylmethionine Dependent Methyltransferases in the Anhydrobiotic Midge
by Ruslan Deviatiiarov, Rustam Ayupov, Alexander Laikov, Elena Shagimardanova, Takahiro Kikawada and Oleg Gusev
Insects 2020, 11(9), 634; https://doi.org/10.3390/insects11090634 - 16 Sep 2020
Cited by 4 | Viewed by 2698
Abstract
Multiple co-localized paralogs of genes in Polypedilum vanderplanki’s genome have strong transcriptional response to dehydration and considered to be a part of adaptation machinery at the larvae stage. One group of such genes represented by L-isoaspartate O-methyltransferases (PIMT). In order to highlight specific [...] Read more.
Multiple co-localized paralogs of genes in Polypedilum vanderplanki’s genome have strong transcriptional response to dehydration and considered to be a part of adaptation machinery at the larvae stage. One group of such genes represented by L-isoaspartate O-methyltransferases (PIMT). In order to highlight specific role of PIMT paralogization in desiccation tolerance of the larvae we annotated and compared S-adenosylmethionine (SAM) dependent methyltransferases of four insect species. From another side we applied co-expression analysis in desiccation/rehydration time course and showed that PIMT coding genes could be separated into five clusters by expression profile. We found that among Polypedilum vanderplanki’s PIMTs only PIMT1 and PIMT2 have enzymatic activity in normal physiological conditions. From in silico analysis of the protein structures we found two highly variable regions outside of the active center, but also amino acid substitutions which may affect SAM stabilization. Overall, in this study we demonstrated features of Polypedilum vanderplanki’s PIMT coding paralogs related to different roles in desiccation tolerance of the larvae. Our results also suggest a role of different SAM-methyltransferases in the adaptation, including GSMT, JHAMT, and candidates from other classes, which could be considered in future studies. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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14 pages, 2967 KiB  
Article
De Novo Transcriptomic and Metabolomic Analyses Reveal the Ecological Adaptation of High-Altitude Bombus pyrosoma
by Yanjie Liu, Huiyue Zhao, Qihua Luo, Yadong Yang, Guangshuo Zhang, Zhiyong Zhou, Muhammad Naeem and Jiandong An
Insects 2020, 11(9), 631; https://doi.org/10.3390/insects11090631 - 14 Sep 2020
Cited by 9 | Viewed by 2917
Abstract
Bombus pyrosoma is one of the most abundant bumblebee species in China, with a distribution range of very varied geomorphology and vegetation, which makes it an ideal pollinator species for research into high-altitude adaptation. Here, we sequenced and assembled transcriptomes of B. pyrosoma [...] Read more.
Bombus pyrosoma is one of the most abundant bumblebee species in China, with a distribution range of very varied geomorphology and vegetation, which makes it an ideal pollinator species for research into high-altitude adaptation. Here, we sequenced and assembled transcriptomes of B. pyrosoma from the low-altitude North China Plain and the high-altitude Tibet Plateau. Subsequent comparative analysis of de novo transcriptomes from the high- and low-altitude groups identified 675 common upregulated genes (DEGs) in the high-altitude B. pyrosoma. These genes were enriched in metabolic pathways and corresponded to enzyme activities involved in energy metabolism. Furthermore, according to joint analysis with comparative metabolomics, we suggest that the metabolism of coenzyme A (CoA) and the metabolism and transport of energy resources contribute to the adaptation of high-altitude B. pyrosoma. Meanwhile, we found many common upregulated genes enriched in the Toll and immune deficiency (Imd)signaling pathways that act as important immune defenses in insects, and hypoxia and cold temperatures could induce the upregulation of immune genes in insects. Therefore, we suppose that the Toll and Imd signaling pathways also participated in the high-altitude adaptation of B. pyrosoma. Like other organisms, we suggest that the high-altitude adaptation of B. pyrosoma is controlled by diverse mechanisms. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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17 pages, 1933 KiB  
Article
Divergence of Desiccation-Related Traits in Sitobion avenae from Northwestern China
by Yujing Yang, Deguang Liu, Xiaoming Liu, Biyao Wang and Xiaoqin Shi
Insects 2020, 11(9), 626; https://doi.org/10.3390/insects11090626 - 11 Sep 2020
Cited by 3 | Viewed by 2081
Abstract
The impact of drought on insects has become increasingly evident in the context of global climate change, but the physiological mechanisms of aphids’ responses to desiccating environments are still not well understood. We sampled the wheat aphid Sitobion avenae (Fabricius) (Hemiptera: Aphididae) from [...] Read more.
The impact of drought on insects has become increasingly evident in the context of global climate change, but the physiological mechanisms of aphids’ responses to desiccating environments are still not well understood. We sampled the wheat aphid Sitobion avenae (Fabricius) (Hemiptera: Aphididae) from arid areas of northwestern China. Both desiccation-resistant and -nonresistant genotypes were identified, providing direct evidence of genetic divergence in desiccation resistance of S. avenae. Resistant genotypes of wingless S. avenae showed longer survival time and LT50 under the desiccation stress (i.e., 10% relative humidity) than nonresistant genotypes, and wingless individuals tended to have higher desiccation resistance than winged ones. Both absolute and relative water contents did not differ between the two kinds of genotypes. Resistant genotypes had lower water loss rates than nonresistant genotypes for both winged and wingless individuals, suggesting that modulation of water loss rates could be the primary strategy in resistance of this aphid against desiccation stress. Contents of cuticular hydrocarbons (CHC) (especially methyl-branched alkanes) showed significant increase for both resistant and nonresistant genotypes after exposure to the desiccation stress for 24 h. Under desiccation stress, survival time was positively correlated with contents of methyl-branched alkanes for resistant genotypes. Thus, the content of methyl-branched alkanes and their high plasticity could be closely linked to water loss rate and desiccation resistance in S. avenae. Our results provide insights into fundamental aspects and underlying mechanisms of desiccation resistance in aphids, and have significant implications for the evolution of aphid populations in the context of global warming. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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Review

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21 pages, 1092 KiB  
Review
Deciphering the Biological Enigma—Genomic Evolution Underlying Anhydrobiosis in the Phylum Tardigrada and the Chironomid Polypedilum vanderplanki
by Yuki Yoshida and Sae Tanaka
Insects 2022, 13(6), 557; https://doi.org/10.3390/insects13060557 - 19 Jun 2022
Cited by 3 | Viewed by 3321
Abstract
Anhydrobiosis, an ametabolic dehydrated state triggered by water loss, is observed in several invertebrate lineages. Anhydrobiotes revive when rehydrated, and seem not to suffer the ultimately lethal cell damage that results from severe loss of water in other organisms. Here, we review the [...] Read more.
Anhydrobiosis, an ametabolic dehydrated state triggered by water loss, is observed in several invertebrate lineages. Anhydrobiotes revive when rehydrated, and seem not to suffer the ultimately lethal cell damage that results from severe loss of water in other organisms. Here, we review the biochemical and genomic evidence that has revealed the protectant molecules, repair systems, and maintenance pathways associated with anhydrobiosis. We then introduce two lineages in which anhydrobiosis has evolved independently: Tardigrada, where anhydrobiosis characterizes many species within the phylum, and the genus Polypedilum, where anhydrobiosis occurs in only two species. Finally, we discuss the complexity of the evolution of anhydrobiosis within invertebrates based on current knowledge, and propose perspectives to enhance the understanding of anhydrobiosis. Full article
(This article belongs to the Special Issue The Adaptations of Arthropods to Extreme Environments)
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