The induction of anhydrobiosis in the sleeping chironomid: Current status of our knowledge

Abstract

An African chironomid, Polypedilum vanderplanki, is the only insect known to be capable of extreme desiccation tolerance, or anhydrobiosis. In the 1950s and 1960s, Hinton strenuously studied anhydrobiosis in this insect from a physiological standpoint; however, nobody has afterward investigated the phenomenon. In 2000, research on mechanisms underlying anhydrobiosis was resumed due to successful establishment of a rearing system for P. vanderplanki. This review is focused on the latest findings on the physiological and molecular mechanisms underlying the induction of anhydrobiosis in P. vanderplanki. Early experiments demonstrated that the induction of anhydrobiosis was possible in isolated tissues and independent from the control of central nervous system. However, to achieve successful anhydrobiosis, larvae need a slow regime of desiccation, allowing them to synthesize molecules, which will protect cells and tissues against the deleterious effects of dehydration. Trehalose, a nonreducing disaccharide, which accumulates in P. vanderplanki larvae up to 20% of the dry body mass, is thought to replace the water in its tissues. Similarly, highly hydrophilic proteins called the late embryogenesis abundant (LEA) proteins are expressed in huge quantities and act as a molecular shield to protect biological molecules against aggregation and denaturation. This function is shared by heat shock proteins, which are also upregulated during the desiccation process. At the same time, desiccating larvae express various antioxidant molecules and enzymes, to cope with the massive oxidative stress, which is responsible for general damage to membranes, proteins, and DNA in dehydrating cells. Finally, specific water channels, called aquaporins, accelerate dehydration, and trehalose together with LEA proteins forms a glassy matrix, which protects the biological molecules and the structural integrity of larvae in the anhydrobiotic state. © 2011 IUBMB IUBMB Life, 63(6): 419–429, 2011

Mechanistic underpinnings of dehydration stress in the American dog tick revealed through RNA-Seq and metabolomics

“…We found that D. variabilis exhibit a suite of biochemical and molecular responses that likely improves their survival during dehydration. Although we studied a single tick species, many of the responses, including up-regulation of stressresponse and proteolysis-related genes, are common across a diverse range of arthropods (Benoit and Denlinger, 2010;Cornette and Kikawada, 2011;King and MacRae, 2015;Teets et al, 2012), suggesting that our findings could be applicable to ticks in general; however, further study is needed to verify that all ticks respond similarly to dehydration. Despite these efforts to reduce stress, the ability of ticks to cope with desiccation is not particularly extraordinary, and their tolerance of ∼30% body water loss (Yoder et al, 2012) is similar to that of many terrestrial arthropods (Hadley, 1994).…”

“…Arthropods have a variety of mechanisms for preventing and tolerating dehydration-associated damage, including changes in the expression of proteins such as heat shock proteins, antioxidant enzymes and aquaporins (Benoit and Denlinger, 2010;Cornette and Kikawada, 2011;King and MacRae, 2015). Additionally, accumulation of various molecules, including trehalose and glycerol, can have protective effects during dehydration by acting to prevent damage to cellular components (Michaud et al, 2008;Watanabe, 2006;Yoder et al, 2006a).…”

Chironomid Midges (Diptera, Chironomidae) Show Extremely Small Genome Sizes

“…In our research group, we have been studying for a decade extreme desiccation tolerance, known as anhydrobiosis, in the African sleeping chironomid, Polypedilum vanderplanki (Hinton, 1951(Hinton, , 1960a(Hinton, , 1960bWatanabe, 2006). The expression of various chaperone proteins, antioxidants, and the ultimate vitrification of a trehalose matrix have been shown to be essential for successful anhydrobiosis (Kikawada et al, 2006;Sakurai et al, 2008;Cornette et al, 2010;Cornette and Kikawada, 2011). Recently, genomic DNA was shown to experience severe damage during anhydrobiosis and these damages were repaired slowly after rehydration .…”

Salinity influence on chironomid larvae (Diptera, Chironomidae) in the Crimean hypersaline lakes

“…Немногочисленные находки личинок при 320 -340 г/л не позволяют сделать однозначный вывод о том, что они могут нормально функционировать при такой солёности. Ряд видов хирономид может длительно находиться в состоянии ангидробиоза (Cornette, Kikawada, 2011). Возможно, некоторые стадии B. noctivagus могут переходить к ан-гидробиозу при высыхании или в условиях очень высокой солёности.…”

“…Личинки некоторых видов Chironomidae способны находиться в неактивном со-стоянии ангидробиоза длительное время (Suemoto et al, 2004), вид Polypedilum vanderplanki Hinton, 1951 -до 17 лет (Cornette, Kikawada, 2011). Можно предполо-жить, что это характерно и для личинок B. noctivagus.…”