Function and immuno-localization of aquaporins in the Antarctic midge Belgica antarctica

Yi, Shu‐Xia; Benoit, Joshua B.; Elnitsky, Michael A.; Kaufmann, Nancy; Brodsky, Jeffrey L.; Zeidel, Mark L.; Denlinger, David L.; Lee, Richard

doi:10.1016/j.jinsphys.2011.02.006

Cited by 36 publications

(43 citation statements)

References 53 publications

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“…AQPs can be divided into two groups that either transport only water or that transport water, glycerol, urea and other small metabolites [23], [24], [26], [30]. AQPs are critical for diuresis after blood feeding and dehydration tolerance in mosquitoes [28], [29], cold and freezing tolerance in various insects [31]–[35] and promote anhydrobiosis in the African sleeping midge [36], [37]. Previous EST projects on tsetse flies have demonstrated the expression of AQPs in many tissues [38]–[40], but the physiological roles of these channel proteins, particularly in relation to viviparous reproduction and blood feeding, have not been determined.…”

Section: Introductionmentioning

confidence: 99%

Aquaporins Are Critical for Provision of Water during Lactation and Intrauterine Progeny Hydration to Maintain Tsetse Fly Reproductive Success

et al. 2014

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Tsetse flies undergo drastic fluctuations in their water content throughout their adult life history due to events such as blood feeding, dehydration and lactation, an essential feature of the viviparous reproductive biology of tsetse. Aquaporins (AQPs) are transmembrane proteins that allow water and other solutes to permeate through cellular membranes. Here we identify tsetse aquaporin (AQP) genes, examine their expression patterns under different physiological conditions (blood feeding, lactation and stress response) and perform functional analysis of three specific genes utilizing RNA interference (RNAi) gene silencing. Ten putative aquaporins were identified in the Glossina morsitans morsitans (Gmm) genome, two more than has been previously documented in any other insect. All organs, tissues, and body parts examined had distinct AQP expression patterns. Two AQP genes, gmmdripa and gmmdripb ( = gmmaqp1a and gmmaqp1b) are highly expressed in the milk gland/fat body tissues. The whole-body transcript levels of these two genes vary over the course of pregnancy. A set of three AQPs (gmmaqp5, gmmaqp2a, and gmmaqp4b) are expressed highly in the Malpighian tubules. Knockdown of gmmdripa and gmmdripb reduced the efficiency of water loss following a blood meal, increased dehydration tolerance and reduced heat tolerance of adult females. Knockdown of gmmdripa extended pregnancy length, and gmmdripb knockdown resulted in extended pregnancy duration and reduced progeny production. We found that knockdown of AQPs increased tsetse milk osmolality and reduced the water content in developing larva. Combined knockdown of gmmdripa, gmmdripb and gmmaqp5 extended pregnancy by 4–6 d, reduced pupal production by nearly 50%, increased milk osmolality by 20–25% and led to dehydration of feeding larvae. Based on these results, we conclude that gmmDripA and gmmDripB are critical for diuresis, stress tolerance and intrauterine lactation through the regulation of water and/or other uncharged solutes.

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Section: Introductionmentioning

confidence: 99%

Aquaporins Are Critical for Provision of Water during Lactation and Intrauterine Progeny Hydration to Maintain Tsetse Fly Reproductive Success

et al. 2014

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“…Although our recent work on B. antarctica has revealed several key molecular mechanisms of dehydration tolerance, including expression of heat shock proteins (11), aquaporins (12,13), and metabolic genes (14), we lack a comprehensive understanding of the genes and pathways involved in extreme dehydration tolerance. To date, only three studies have examined large-scale transcriptional changes in response to dehydration in insects, all of which were conducted on tropical species.…”

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confidence: 99%

Gene expression changes governing extreme dehydration tolerance in an Antarctic insect

Teets¹,

Peyton

Colinet

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Among terrestrial organisms, arthropods are especially susceptible to dehydration, given their small body size and high surface area to volume ratio. This challenge is particularly acute for polar arthropods that face near-constant desiccating conditions, as water is frozen and thus unavailable for much of the year. The molecular mechanisms that govern extreme dehydration tolerance in insects remain largely undefined. In this study, we used RNA sequencing to quantify transcriptional mechanisms of extreme dehydration tolerance in the Antarctic midge, Belgica antarctica, the world's southernmost insect and only insect endemic to Antarctica. Larvae of B. antarctica are remarkably tolerant of dehydration, surviving losses up to 70% of their body water. Gene expression changes in response to dehydration indicated up-regulation of cellular recycling pathways including the ubiquitin-mediated proteasome and autophagy, with concurrent down-regulation of genes involved in general metabolism and ATP production. Metabolomics results revealed shifts in metabolite pools that correlated closely with changes in gene expression, indicating that coordinated changes in gene expression and metabolism are a critical component of the dehydration response. Finally, using comparative genomics, we compared our gene expression results with a transcriptomic dataset for the Arctic collembolan, Megaphorura arctica. Although B. antarctica and M. arctica are adapted to similar environments, our analysis indicated very little overlap in expression profiles between these two arthropods. Whereas several orthologous genes showed similar expression patterns, transcriptional changes were largely species specific, indicating these polar arthropods have developed distinct transcriptional mechanisms to cope with similar desiccating conditions. physiological ecology | environmental stress

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“…The Journal of Experimental Biology (2014) antibodies from different species, and some of these were stress inducible (Yi et al, 2011). However, the sequence identity of these aquaporin genes has not been established.…”

Section: Reviewmentioning

confidence: 99%

“…However, mRNA expression did not change in response to dehydration, so it is unclear what, if any, role this gene plays in mediating stress tolerance. A second study of B. antarctica aquaporins found immunoreactivity to four different aquaporin antibodies from different species, and some of these were stress inducible (Yi et al, 2011). However, the sequence identity of these aquaporin genes has not been established.…”

Section: Reviewmentioning

confidence: 99%

“…Most adaptations described in Antarctic arthropods, such as accumulation of osmoprotectants (e.g. Baust and Lee, 1983) and the role of aquaporins during freeze tolerance (Yi et al, 2011), have been previously described in temperate species. Thus, despite recent advances in the molecular physiology of Antarctic arthropods, unique Antarctic adaptations, if they exist, have been elusive to physiologists.…”

Section: Reviewmentioning

confidence: 99%

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Surviving in a frozen desert: environmental stress physiology of terrestrial Antarctic arthropods

Teets

Denlinger

2014

Journal of Experimental Biology

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Abiotic stress is one of the primary constraints limiting the range and success of arthropods, and nowhere is this more apparent than Antarctica. Antarctic arthropods have evolved a suite of adaptations to cope with extremes in temperature and water availability. Here, we review the current state of knowledge regarding the environmental physiology of terrestrial arthropods in Antarctica. To survive low temperatures, mites and Collembola are freeze-intolerant and rely on deep supercooling, in some cases supercooling below -30°C. Also, some of these microarthropods are capable of cryoprotective dehydration to extend their supercooling capacity and reduce the risk of freezing. In contrast, the two best-studied Antarctic insects, the midges Belgica antarctica and Eretmoptera murphyi, are freezetolerant year-round and rely on both seasonal and rapid coldhardening to cope with decreases in temperature. A common theme among Antarctic arthropods is extreme tolerance of dehydration; some accomplish this by cuticular mechanisms to minimize water loss across their cuticle, while a majority have highly permeable cuticles but tolerate upwards of 50-70% loss of body water. Molecular studies of Antarctic arthropod stress physiology are still in their infancy, but several recent studies are beginning to shed light on the underlying mechanisms that govern extreme stress tolerance. Some common themes that are emerging include the importance of cuticular and cytoskeletal rearrangements, heat shock proteins, metabolic restructuring and cell recycling pathways as key mediators of cold and water stress in the Antarctic. KEY WORDS: Antarctica, Cold tolerance, Dehydration, Environmental stress, Physiology IntroductionEnvironmental stress, in the form of both biotic and abiotic stress, is one of the primary constraints governing the abundance and distribution of terrestrial arthropods. While insects on all continents encounter some form of environmental stress, perhaps nowhere are the environmental onslaughts more challenging than the continent of Antarctica. Even in maritime Antarctica, where proximity to the sea limits temperature extremes, winter lows exceed -40°C and subzero temperatures can be experienced any time of year . Furthermore, water is frozen and biologically unavailable for much of the year, thus water availability is perhaps the biggest challenge confronting terrestrial arthropods in Antarctica (Kennedy, 1993). Whereas arthropods are the predominant terrestrial life form on Earth, only a handful of species have successfully established in Antarctica, and most of these are restricted to maritime regions (Convey, 1996a; Convey, 2013 In this review, we summarize the limits and mechanisms of environmental stress tolerance in Antarctic arthropods. In particular, we focus on the biochemical and molecular underpinnings of the stress response in Antarctic arthropods. As non-model (not to mention difficult to access) species, molecular studies of Antarctic arthropods have been limited in scope. However, recent advances i...

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Function and immuno-localization of aquaporins in the Antarctic midge Belgica antarctica

Cited by 36 publications

References 53 publications

Aquaporins Are Critical for Provision of Water during Lactation and Intrauterine Progeny Hydration to Maintain Tsetse Fly Reproductive Success

Aquaporins Are Critical for Provision of Water during Lactation and Intrauterine Progeny Hydration to Maintain Tsetse Fly Reproductive Success

Gene expression changes governing extreme dehydration tolerance in an Antarctic insect

Surviving in a frozen desert: environmental stress physiology of terrestrial Antarctic arthropods

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