Impact of salt-contaminated freshwater on osmoregulation and tracheal gill function in nymphs of the mayfly Hexagenia rigida

Nowghani, Fargol; Chen, Chun-Chih; Jonusaite, Sima; Watson-Leung, Trudy; Kelly, Scott P.; Donini, Andrew

doi:10.1016/j.aquatox.2019.03.019

Cited by 18 publications

(16 citation statements)

References 60 publications

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“…6 and 8), may be an indication that the exocrine glands develop from the same homologous precursors. This possibility is consistent with the facts that the gills of mayfly larvae, and the epipods/gills of the crustacean Artemia, have osmoregulatory functions (50)(51)(52) and, moreover, the gills and exocrine glands of crustaceans share a similar genetic network (i.e., they both express trh and vvl) (52-54). Genetic and mo-lecular studies utilizing semiaquatic insects that possess trachea, gills, and osmoregulatory organs (55), may be especially informative in elucidating the developmental mechanisms that facilitated the evolution of a tracheal system in terrestrial arthropods.…”

Section: Significancesupporting

confidence: 85%

A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development

Hanna

Popadić

2020

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

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The diversity in the organization of the tracheal system is one of the drivers of insect evolutionary success; however, the genetic mechanisms responsible are yet to be elucidated. Here, we highlight the advantages of utilizing hemimetabolous insects, such as the milkweed bug Oncopeltus fasciatus, in which the final adult tracheal patterning can be directly inferred by examining its blueprint in embryos. By reporting the expression patterns, functions, and Hox gene regulation of trachealess (trh), ventral veinless (vvl), and cut (ct), key genes involved in tracheal development, this study provides important insights. First, Hox genes function as activators, modifiers, and suppressors of trh expression, which in turn results in a difference between the thoracic and abdominal tracheal organization. Second, spiracle morphogenesis requires the input of both trh and ct, where ct is positively regulated by trh. As Hox genes regulate trh, we can now mechanistically explain the previous observations of their effects on spiracle formation. Third, the default state of vvl expression in the thorax, in the absence of Hox gene expression, features three lateral cell clusters connected to ducts. Fourth, the exocrine scent glands express vvl and are regulated by Hox genes. These results extend previous findings [Sánchez-Higueras et al., 2014], suggesting that the exocrine glands, similar to the endocrine, develop from the same primordia that give rise to the trachea. The presence of such versatile primordia in the miracrustacean ancestor could account for the similar gene networks found in the glandular and respiratory organs of both insects and crustaceans.

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Section: Significancesupporting

confidence: 85%

A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development

Hanna

Popadić

2020

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

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“…Other studies have not observed differences in ionocyte numbers as a function of environmental conditions. For example, Nowghani et al found no impact of similar but sub-lethal levels of NaCl on ionocyte density in the mayfly Hexagenia rigida [74]; however, this study was conducted on a relatively shorter timescale (7 days). Berrill et al [75] did not observe differences in ionocyte densities in a variety of mayfly species associated with pH stress.…”

Section: Discussionmentioning

confidence: 72%

“…For example, Nowghani et al . found no impact of similar but sub-lethal levels of NaCl on ionocyte density in the mayfly Hexagenia rigida [ 74 ]; however, this study was conducted on a relatively shorter timescale (7 days). Berrill et al .…”

Section: Discussionmentioning

confidence: 99%

The acclimatory response of the mayfly Neocloeon triangulifer to dilute conditions is linked to the plasticity of sodium transport

Cochran

Buchwalter

2022

Proc. R. Soc. B.

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Relative to a growing body of knowledge about the negative consequences of freshwater salinization, little is known about how aquatic insects respond to progressively ion-poor conditions. Here, we examined life-history and physiological acclimation in Neocloeon triangulifer by rearing nymphs from 1-day post-egg hatch to adulthood across a gradient of decreasing Na concentrations (15, 8, 4, 2 and 1 mg l −1 Na). We found no significant changes in survival, growth, development time and whole-body Na content across these treatments. Radiotracer data revealed that nymphs acclimated to their dilute exposures by increasing their rates of Na uptake and were able to maintain a relatively narrow range of uptake rates (±s.e.m.) of 38.5 ± 4.2 µg Na g −1 h −1 across all treatments. By contrast, the Na uptake rates observed in naive nymphs were much more concentration dependent. This acclimatory response is partially explained by differences in ionocyte counts on the gills of nymphs reared under different salinities. Acclimated nymphs were surprisingly less retentive of their sodium composition when subjected to deionized water challenge. By contrasting our findings with a previous N. triangulifer salinity acclimation study, we show a physiological affinity for dilute conditions in this emerging mayfly model.

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“…Slides were mounted using with mount media containing DAPI for nuclei staining (ProLong Gold antifade reagent, Life Technologies, Burlington, ON). Fluorescence images were captured on an Olympus IX81 inverted microscope (Olympus Canada, Richmond Hill, ON, Canada) equipped with an X-CITE 120XL Fluorescent Illuminator (X-CITE, Mississauga, ON, Canada) 41,46 . Images were merged using ImageJ 1.50i software (National Institutes of Health, Bethesda, MD, USA).…”

Section: Methodsmentioning

confidence: 99%

Development of Aedes aegypti (Diptera: Culicidae) mosquito larvae in high ammonia sewage in septic tanks causes alterations in ammonia excretion, ammonia transporter expression, and osmoregulation

Durant

Donini

2019

Sci Rep

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Larvae of the disease vector mosquito, Aedes aegypti (L.) readily develop in ammonia rich sewage in the British Virgin Islands. To understand how the larvae survive in ammonia levels that are lethal to most animals, an examination of ammonia excretory physiology in larvae collected from septic-water and freshwater was carried out. A. aegypti larvae were found to be remarkably plastic in dealing with high external ammonia through the modulation of NH4+ excretion at the anal papillae, measured using the scanning ion-selective electrode technique (SIET), and NH4+ secretion in the primary urine by the Malpighian tubules when developing in septicwater. Ammonia transporters, Amt and Rh proteins, are expressed in ionoregulatory and excretory organs, with increases in Rh protein, Na+-K+-ATPase, and V-type-H+-ATPase expression observed in the Malpighian tubules, hindgut, and anal papillae in septic-water larvae. A comparative approach using laboratory A. aegypti larvae reared in high ammonia septic-water revealed similar responses to collected A. aegypti with regard to altered ammonia secretion and hemolymph ion composition. Results suggest that the observed alterations in excretory physiology of larvae developing in septic-water is a consequence of the high ammonia levels and that A. aegypti larvae may rely on ammonia transporting proteins coupled to active transport to survive in septic-water.

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Impact of salt-contaminated freshwater on osmoregulation and tracheal gill function in nymphs of the mayfly Hexagenia rigida

Cited by 18 publications

References 60 publications

A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development

A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development

The acclimatory response of the mayfly Neocloeon triangulifer to dilute conditions is linked to the plasticity of sodium transport

Development of Aedes aegypti (Diptera: Culicidae) mosquito larvae in high ammonia sewage in septic tanks causes alterations in ammonia excretion, ammonia transporter expression, and osmoregulation

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