The mayfly <i>Neocloeon triangulifer</i> senses decreasing oxygen availability (<i>P</i>O2) and responds by reducing ion uptake and altering gene expression

Oxygen availability is central to the energetic budget of aquatic animals and may vary naturally and/or in response to anthropogenic activities. Yet, we know little about how oxygen availability is linked to fundamental processes such as ion transport in aquatic insects. We hypothesized and observed that ion (22Na and 35SO4) uptake would be significantly decreased at O2 partial pressures below the mean critical level (Pcrit, 5.4 kPa) where metabolic rate (ṀO2) is compromised and ATP production is limited. However, we were surprised to observe marked reductions in ion uptake at oxygen partial pressures well above Pcrit, where ṀO2 was stable. For example, SO4 uptake decreased by 51% at 11.7 kPa and 82% at Pcrit (5.4 kPa) while Na uptake decreased by 19% at 11.7 kPa and 60% at Pcrit. Nymphs held for longer time periods at reduced PO2 exhibited stronger reductions in ion uptake rates. Fluids from whole-body homogenates exhibited a 29% decrease in osmolality in the most hypoxic condition. The differential expression of atypical guanylate cyclase (gcy-88e) in response to changing PO2 conditions provides evidence for its potential role as an oxygen sensor. Several ion transport genes (e.g. chloride channel and sodium-potassium ATPase) and hypoxia-associated genes (e.g. ldh and egl-9) were also impacted by decreased oxygen availability. Together, the results of our work suggest that N. triangulifer can sense decreased oxygen availability and perhaps conserves energy accordingly, even when ṀO2 is not impacted.

Authors

Institutions

Publication Details

Journal
Journal of Experimental Biology
Published
2024-10-18
DOI
https://doi.org/10.1242/jeb.247916
Citations
2
Primary Topic
Physiological and biochemical adaptations
Type
article
Field-Weighted Citation Impact
0.92

Funders

Controls
|||
ALL TIME
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
article

The mayfly Neocloeon triangulifer senses decreasing oxygen availability (PO2) and responds by reducing ion uptake and altering gene expression

David B. Buchwalter, Jamie K. Cochran
2 citations
Journal of Experimental Biology
Physiological and biochemical adaptations
0.92
article

The mayfly Neocloeon triangulifer senses decreasing oxygen availability (PO2) and responds by reducing ion uptake and altering gene expression

David B. Buchwalter, Jamie K. Cochran
article en
2 citations

Abstract

Oxygen availability is central to the energetic budget of aquatic animals and may vary naturally and/or in response to anthropogenic activities. Yet, we know little about how oxygen availability is linked to fundamental processes such as ion transport in aquatic insects. We hypothesized and observed that ion (22Na and 35SO4) uptake would be significantly decreased at O2 partial pressures below the mean critical level (Pcrit, 5.4 kPa) where metabolic rate (ṀO2) is compromised and ATP production is limited. However, we were surprised to observe marked reductions in ion uptake at oxygen partial pressures well above Pcrit, where ṀO2 was stable. For example, SO4 uptake decreased by 51% at 11.7 kPa and 82% at Pcrit (5.4 kPa) while Na uptake decreased by 19% at 11.7 kPa and 60% at Pcrit. Nymphs held for longer time periods at reduced PO2 exhibited stronger reductions in ion uptake rates. Fluids from whole-body homogenates exhibited a 29% decrease in osmolality in the most hypoxic condition. The differential expression of atypical guanylate cyclase (gcy-88e) in response to changing PO2 conditions provides evidence for its potential role as an oxygen sensor. Several ion transport genes (e.g. chloride channel and sodium-potassium ATPase) and hypoxia-associated genes (e.g. ldh and egl-9) were also impacted by decreased oxygen availability. Together, the results of our work suggest that N. triangulifer can sense decreased oxygen availability and perhaps conserves energy accordingly, even when ṀO2 is not impacted.

Journal of Experimental BiologyVol. 227(23)
North Carolina State University (US)
North Carolina State University
Life below water
Openalex Percentile: Top 22%
Physiological and biochemical adaptations
0.92
AI Navigator

Ask Laika to Summarize, Analyze, and Connect papers live on the map.

Summarize Papers & Methodologies

Extract key findings, datasets, and comparative methods across publications.

Benchmark Rankings & Visual Analytics

Rank top research institutions, authors, funders, topics, and journals by Field-Weighted Citation Impact (FWCI) and paper volume with instant charts.

Connect Distant Disciplines

Bridge topological clusters on the map to find hidden collaborative intersections.