NHA1 is a cation/proton antiporter essential for the water-conserving functions of the rectal complex in Tribolium castaneum

Author:

Naseem Muhammad T.1ORCID,Beaven Robin2ORCID,Koyama Takashi1ORCID,Naz Sehrish1,Su Sheng-yuan2,Leader David P.3ORCID,A. Klaerke Dan4,Calloe Kirstine4ORCID,Denholm Barry2ORCID,Halberg Kenneth V.1ORCID

Affiliation:

1. Department of Biology, Section for Cell and Neurobiology, University of Copenhagen, Copenhagen DK-2100, Denmark

2. Deanery of Biomedical Sciences, College of Medicine and Veterinary Medicine, University of Edinburgh, Edinburgh EH8 9AG, UK

3. Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK

4. Department of Veterinary and Animal Sciences, Section for Pathobiological Sciences, University of Copenhagen DK-1870, Frederiksberg, Denmark

Abstract

More than half of all extant metazoan species on earth are insects. The evolutionary success of insects is linked with their ability to osmoregulate, suggesting that they have evolved unique physiological mechanisms to maintain water balance. In beetles (Coleoptera)—the largest group of insects—a specialized rectal (“cryptonephridial”) complex has evolved that recovers water from the rectum destined for excretion and recycles it back to the body. However, the molecular mechanisms underpinning the remarkable water-conserving functions of this system are unknown. Here, we introduce a transcriptomic resource, BeetleAtlas.org, for the exceptionally desiccation-tolerant red flour beetle  Tribolium castaneum,  and demonstrate its utility by identifying a cation/H +  antiporter (NHA1) that is enriched and functionally significant in the  Tribolium  rectal complex. NHA1 localizes exclusively to a specialized cell type, the leptophragmata, in the distal region of the Malpighian tubules associated with the rectal complex. Computational modeling and electrophysiological characterization in  Xenopus oocytes  show that NHA1 acts as an electroneutral K + /H +  antiporter. Furthermore, genetic silencing of  Nha1  dramatically increases excretory water loss and reduces organismal survival during desiccation stress, implying that NHA1 activity is essential for maintaining systemic water balance. Finally, we show that Tiptop, a conserved transcription factor, regulates NHA1 expression in leptophragmata and controls leptophragmata maturation, illuminating the developmental mechanism that establishes the functions of this cell. Together, our work provides insights into the molecular architecture underpinning the function of one of the most powerful water-conserving mechanisms in nature, the beetle rectal complex.

Funder

Villum Fonden

Danmarks Frie Forskningsfond

Ragna Rask-Nielsens Foundation

Carlsbergfondet

Carnegie Dunfermline Trust

Leverhulme Trust

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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