The dromedary camel (Camelus dromedarius) has considerable economic and cultural importance in the Middle East and North Africa. The “ship of the desert” has been the most important domesticated species in these regions for millennia. As an adaptation to long-term drought conditions in the desert environment, the camel has evolved robust mechanisms to maintain water homeostasis. At the level of the kidney, the camel is capable of producing a low volume of highly concentrated urine via efficient water reabsorption, especially when challenged by water deprivation. The water reabsorption from the pre-urine is mediated by the hormones arginine vasopressin (AVP) and oxytocin (OXT), two key osmo-regulators that are produced in the hypothalamic supraoptic nucleus (SON) and paraventricular nucleus (PVN) in the brain.
To reveal the physiological mechanisms underlying water homeostasis under the tremendous pressures of the hot desert environment, our lab decided to look at the nature’s water conserving wonder, the camel, to seek answers to specialisations that ensure survival in desert using omics techniques and advanced bioinformatics. Thus, an exciting collaborative project developed between Professor Abdu Adem (United Arab Emirates University) and Professor David Murphy (University of Bristol). The mutual goal for the two laboratories was to study the kidney and brain of the Arabian dromedary camel challenged by long-term water deprivation and subsequent rapid rehydration. The physiological experiments were carried out with ranch-housed camel outside Al Ain, United Arab Emirates, during the hot months (April and May) of 2016, under careful veterinary supervision to ensure animal welfare. Having reported transcriptomic and proteomic adaptations to water deprivation in the camel kidney in 2021 (please visit this nature portfolio blog by Fernando Alvira Iraizoz for more information), we turned our attention to the neuroendocrine mechanisms that orchestrate the response to water deprivation in the camel hypothalamus. This is the first time that the camel hypothalamus has been so extensively studied in terms of its adaptations to the desert environment.
My enthusiasm in camels was developed during my past residence in the northwest China, where I encountered free-range farming of Bactrian camels when traveling to the Kumtag Desert and Gobi deserts. Similar to the important roles played by dromedary camels to provide milk, meat, transportation and entertainment to people in North and East Africa, the Arabian Peninsula and Iran and many Middle Eastern countries, the Bactrian camel is a very important livestock for people from northwest China and Mongolia as well. Additionally, I am concerned about the conservation of one of the critically endangered species in the world - the wild Bactrian camel – which inhabits the deserts of northwest China and southwest Mongolia. How these domestic and wild camels cope with drastic environmental change such as desertification and climate change has become my major interest over the past few years. As an earlier stage researcher, I had background in microbiology as well as applied biosciences and biotechniques before joining the Murphy Lab, so basically, I had limited experience in animal physiology and neuroendocrinology. Luckily, by working together with many amazing colleagues and collaborators, I was equipped with relevant knowledge and techniques that enabled me to vigorously pursue my interest in the Camelid family.
This project studying the transcriptomic plasticity of SON – the hypothalamic osmoregulatory control centre of the dromedary camel – started with three-dimensional mapping of the camel SON (Figure 1, Movie 1) based on the expression of the AVP and OXT mRNAs to facilitate SON sampling. Different from the rodent SONs, the camel SON revealed a distinct spatial structure that including two separate subpopulations of magnocellular cells that make these hormones. We named them the rostral SON and caudal SON, regarding their relative location along the rostral-caudal axis in the brain.
We then compared the transcriptomes of the camel SON under control and water deprived conditions. 209 genes were identified to be significantly changed in expression by water deprivation (Figure 2). By further comparing the WD camel SON transcriptome to our previously published rat transcriptome (Pauža et al., 2021), 80 common differentially expressed genes while 129 were uniquely changed in the camel SON (Figure 3). Further, we identified core gene pathways that are commonly changed in the WD camel and rat (Figure 3), including the pathway “Protein processing in endoplasmic reticulum”. Same as rat, the camel SON may undergo enhanced protein processing that is associated with increased demand of neuropeptide secretion, endoplasmic reticulum stress and unfolded protein response due to the accumulation of unfolded/misfolded protein during WD. Other genes and pathways that are uniquely changed in the WD camel SON (Figure 3) and as such might be indispensable for life in the arid desert were also identified, suggesting that the camel SON may undergo additional structural remodelling in extracellular matrix to promote the synthesis and release of AVP and OXT. The upregulated expression of cellular stress sensor protein IRE1 uniquely in the camel supports the concept that the unfolded protein response is activated in the SON perhaps as a protective mechanism for neurons in chronic WD.
To support the growing interest in osmoregulatory processes inclassic rodent models and more unusual desert animals, my colleague Ben Gillard has set up a multi species/tissue expression analysis app (please visit https://bengillard.shinyapps.io/MultiSpeciesExpression/), where the transcriptomic data of rat, dromedary camel and jerboa (a desert rodent model) is easily accessible. The expression of genes of interest can be retrieved by browsing by gene name in this app. We are keen to receive feedback on this app!
Apart from the camel hypothalamic samples, many other organs and tissues from these animals were collected. These samples are being studied by numerous groups around the globe. Thus, over the coming years, we will present a comprehensive picture of the overall physiological and molecular responses of the camel to WD and subsequent rehydration. This will provide valuable information in the context of desertification and climate change and could be used to forecast and evaluate how different species will adapt to constantly changing environments.