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Fluid Secretion by Malpighian Tubules of Rhodnius prolixus: Neuroendocrine Control With New Insights From a Transcriptome Analysis

ABSTRACT: Rhodnius prolixus (the kissing bug and a major vector of Chagas disease) is an obligate blood feeder that in the case of the fifth instar consumes up to 10 times its unfed body weight in a single 20-minute feed. A post-prandial diuresis is initiated, within minutes of the start of gorging, in order to lower the mass and concentrate the nutrients of the meal. Thus, R. prolixus rapidly excretes a fluid that is high in NaCl content and hypo-osmotic to the hemolymph, thereby eliminating 50% of the volume of the blood meal within 3 hours of gorging. In R. prolixus, as with other insects, the Malpighian tubules play a critical role in diuresis. Malpighian tubules are not innervated, and their fine control comes under the influence of the neuroendocrine system that releases amines and neuropeptides as diuretic or antidiuretic hormones. These hormones act upon the Malpighian tubules via a variety of G protein-coupled receptors linked to second messenger systems that influence ion transporters and aquaporins; thereby regulating fluid secretion. Much has been discovered about the control of diuresis in R. prolixus, and other model insects, using classical endocrinological studies. The post-genomic era, however, has brought new insights, identifying novel diuretic and antidiuretic hormone-signaling pathways whilst also validating many of the classical discoveries. This paper will focus on recent discoveries into the neuroendocrine control of the rapid post-prandial diuresis in R. prolixus, in order to emphasize new insights from a transcriptome analysis of Malpighian tubules taken from unfed and fed bugs.

SUBMITTER: Orchard I

PROVIDER: S-EPMC8426621 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundRhodnius montenegrensis (Triatominae), a potential vector of Chagas disease, was described after R. robustus-like bugs from southwestern Amazonia. Mitochondrial cytb sequence near-identity with sympatric R. robustus (genotype II) raised doubts about the taxonomic status of R. montenegrensis, but comparative studies have reported fairly clear morphological and genetic differences between R. montenegrensis and laboratory stocks identified as R. robustus. Here, we use a transcriptome-based approach to investigate this apparent paradox.ResultsWe retrieved publicly-available transcriptome sequence-reads from R. montenegrensis and from the R. robustus stocks used as the taxonomic benchmark in comparative studies. We (i) aligned transcriptome sequence-reads to mitochondrial (cytb) and nuclear (ITS2, D2-28S and AmpG) query sequences (47 overall) from members of the R. prolixus-R. robustus cryptic-species complex and related taxa; (ii) computed breadth- and depth-coverage for the 259 consensus sequences generated by these alignments; and, for each locus, (iii) appraised query sequences and full-breadth-coverage consensus sequences in terms of nucleotide-sequence polymorphism and phylogenetic relations. We found evidence confirming that R. montenegrensis and R. robustus genotype II are genetically indistinguishable and, hence, implying that they are, in all likelihood, the same species. Furthermore, we found compelling genetic evidence that the benchmark 'R. robustus' stocks used in R. montenegrensis description and in later transcriptome-based comparisons are in fact R. prolixus, although likely mixed to some degree with R. robustus (probably genotype II, a.k.a. R. montenegrensis).ConclusionsWe illustrate how public-domain genetic/transcriptomic data can help address challenging issues in disease-vector systematics. In our case-study, taxonomic confusion apparently stemmed from the misinterpretation of sequence-data analyses and misidentification of taxonomic-benchmark stocks. More generally, and together with previous reports of mixed and/or misidentified Rhodnius spp. laboratory colonies, our results call into question the conclusions of many studies (on morphology, genetics, physiology, behavior, bionomics or interactions with microorganisms including trypanosomes) based on non-genotyped 'R. prolixus' or 'R. robustus' stocks. Correct species identification is a prerequisite for investigating the factors that underlie the physiological, behavioral or ecological differences between primary domestic vectors of Chagas disease, such as R. prolixus, and their sylvatic, medically less-relevant relatives such as R. robustus (s.l.) including R. montenegrensis.

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Fluid Secretion by Malpighian Tubules of Rhodnius prolixus: Neuroendocrine Control With New Insights From a Transcriptome Analysis

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