Ammonia excretion in aquatic invertebrates: new insights and questions

Weihrauch, Dirk; Allen, Garett Joseph Patrick

doi:10.1242/jeb.169219

Cited by 74 publications

(25 citation statements)

References 85 publications

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“…To reveal the excretory mechanism in xenacoelomorphs, we conducted high environmental ammonia (HEA) incubation experiments, as previously performed in a large array of animals (summarized in [5,50]), using I . pulchra because of its availability in sufficient numbers.…”

Section: Resultsmentioning

confidence: 99%

Active mode of excretion across digestive tissues predates the origin of excretory organs

et al. 2019

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Most bilaterian animals excrete toxic metabolites through specialized organs, such as nephridia and kidneys, which share morphological and functional correspondences. In contrast, excretion in non-nephrozoans is largely unknown, and therefore the reconstruction of ancestral excretory mechanisms is problematic. Here, we investigated the excretory mode of members of the Xenacoelomorpha, the sister group to Nephrozoa, and Cnidaria, the sister group to Bilateria. By combining gene expression, inhibitor experiments, and exposure to varying environmental ammonia conditions, we show that both Xenacoelomorpha and Cnidaria are able to excrete across digestive-associated tissues. However, although the cnidarian Nematostella vectensis seems to use diffusion as its main excretory mode, the two xenacoelomorphs use both active transport and diffusion mechanisms. Based on these results, we propose that digestive-associated tissues functioned as excretory sites before the evolution of specialized organs in nephrozoans. We conclude that the emergence of a compact, multiple-layered bilaterian body plan necessitated the evolution of active transport mechanisms, which were later recruited into the specialized excretory organs.

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Section: Resultsmentioning

confidence: 99%

Active mode of excretion across digestive tissues predates the origin of excretory organs

et al. 2019

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“…At physiological pH (∼7.4; pK a =9.4), only 1.7% of total ammonia is present as NH 3 (Weiner and Verlander, 2017). The predominant ionic form, NH 4 + , acts as an H + equivalent that can alter intracellular and extracellular pH when transported (Weihrauch and Allen, 2018). However, the extent to which ammonia transport is used to mitigate changes in pH of internal fluids of aquatic invertebrates remains poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Evidence that Rh proteins in the anal papillae of the freshwater mosquitoAedes aegyptiare involved in the regulation of acid base balance in elevated salt and ammonia environments

Durant

Donini

2018

Journal of Experimental Biology

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Aedes aegypti commonly inhabit ammonia-rich sewage effluents in tropical regions of the world where the adults are responsible for the spread of disease. Studies have shown the importance of the anal papillae of A. aegypti in ion uptake and ammonia excretion. The anal papillae express ammonia transporters and Rhesus (Rh) proteins which are involved in ammonia excretion and studies have primarily focused on understanding these mechanisms in freshwater. In this study, effects of rearing larvae in salt (5 mmol l −1 NaCl) or ammonia (5 mmol l −1 NH 4 Cl) on physiological endpoints of ammonia and ion regulation were assessed. In anal papillae of NaCl-reared larvae, Rh protein expression increased, NHE3 transcript abundance decreased and NH 4 + excretion increased, and this coincided with decreased hemolymph [NH 4 + ] and pH. We propose that under these conditions, larvae excrete more NH 4 + through Rh proteins as a means of eliminating acid from the hemolymph. In anal papillae of NH 4 Clreared larvae, expression of an apical ammonia transporter and the Rh proteins decreased, the activities of NKA and VA decreased and increased, respectively, and this coincided with hemolymph acidification. The results present evidence for a role of Rh proteins in acid-base balance in response to elevated levels of salt, whereby ammonia is excreted as an acid equivalent.

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“…Retention of ammonia and potential ‘ammonia homeostasis’ has been hypothesized as an important acid–base regulatory process that occurs in parallel to HCO 3 − accumulation in some invertebrates such as the American horseshoe crab 65 and the common octopus 66 . Selective retention or excretion of ammonia would require a bi-directional mechanism to be present such as the vesicular trafficking mechanism believed to be generally employed by other marine invertebrates and animals inhabiting buffered environments 19 , 67 – 69 . The vesicular trafficking mechanism hypothesizes that ammonia becomes trapped as NH 4 + in vesicles acidified by either V + -type H + -ATPases (HAT) or Na + /H + exchangers and moved within the cell by the microtubular network 69 .…”

Section: Discussionmentioning

confidence: 99%

“…bones or the haemocoel and shell of calcified invertebrates) 10 , 16 , 17 . Non-bicarbonate buffers such as ammonia, proteins/amino acids, and phosphates generally play an important, but lesser role depending on species 18 , 19 . These compensatory mechanisms are becoming increasingly important to aquatic organisms as dissolution of CO 2 into the world’s waterways continues to decrease environmental pH—a process commonly termed ocean acidification 8 .…”

Section: Introductionmentioning

confidence: 99%

Specialized adaptations allow vent-endemic crabs (Xenograpsus testudinatus) to thrive under extreme environmental hypercapnia

Allen

Kuan

Tseng

et al. 2020

Sci Rep

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Shallow hydrothermal vent environments are typically very warm and acidic due to the mixing of ambient seawater with volcanic gasses (> 92% CO2) released through the seafloor making them potential ‘natural laboratories’ to study long-term adaptations to extreme hypercapnic conditions. Xenograpsus testudinatus, the shallow hydrothermal vent crab, is the sole metazoan inhabitant endemic to vents surrounding Kueishantao Island, Taiwan, where it inhabits waters that are generally pH 6.50 with maximum acidities reported as pH 5.50. This study assessed the acid–base regulatory capacity and the compensatory response of X. testudinatus to investigate its remarkable physiological adaptations. Hemolymph parameters (pH, [HCO3−], $${\text{P}}_{{{\text{CO}}_{2} }}$$PCO2, [NH4+], and major ion compositions) and the whole animal’s rates of oxygen consumption and ammonia excretion were measured throughout a 14-day acclimation to pH 6.5 and 5.5. Data revealed that vent crabs are exceptionally strong acid–base regulators capable of maintaining homeostatic pH against extreme hypercapnia (pH 5.50, 24.6 kPa $${\text{P}}_{{{\text{CO}}_{2} }}$$PCO2) via HCO3−/Cl− exchange, retention and utilization of extracellular ammonia. Intact crabs as well as their isolated perfused gills maintained $${\text{P}}_{{{\text{CO}}_{2} }}$$PCO2tensions below environmental levels suggesting the gills can excrete CO2 against a hemolymph-directed $${\text{P}}_{{{\text{CO}}_{2} }}$$PCO2 gradient. These specialized physiological mechanisms may be amongst the adaptations required by vent-endemic animals surviving in extreme conditions.

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Ammonia excretion in aquatic invertebrates: new insights and questions

Cited by 74 publications

References 85 publications

Active mode of excretion across digestive tissues predates the origin of excretory organs

Active mode of excretion across digestive tissues predates the origin of excretory organs

Evidence that Rh proteins in the anal papillae of the freshwater mosquitoAedes aegyptiare involved in the regulation of acid base balance in elevated salt and ammonia environments

Specialized adaptations allow vent-endemic crabs (Xenograpsus testudinatus) to thrive under extreme environmental hypercapnia

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