The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii

Victoria Matey, Jeffrey G. Richards, Yuxiang Wang, Chris M. Wood, Joe Rogers, Rhiannon Davies, Brent W. Murray, X. Q. Chen, Jizeng Du, Colin J. Brauner

Research output: Contribution to journalArticle

79 Citations (Scopus)

Abstract

Goldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3 mg O2 l-1) for 24 h followed by 12 h recovery in normoxic water (6 mg O2 l-1 at 3200 m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8 h of hypoxia and almost complete by 24 h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water-blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24 h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na+] and [Cl-], respectively, within 12-24 h of hypoxia. Within 12 h of hypoxia exposure, 'wavy-convex'-mitochondria rich cells (MRCs) with large apical crypts and numerous branched microvilli were transformed into small 'shallow-basin' cells with a flattened surface. As the apical membrane of MRCs is the site for active ion uptake from the water, a reduction in apical crypt surface area may have contributed to the progressive reduction in plasma [Na+] and [Cl -] observed during hypoxia. The changes in the macro- and ultra-structure of fish gills, and plasma [Na+] and [Cl-] during hypoxia were reversible, showing partial recovery by 12 h following return to normoxia. Although the large morphological changes in the gill observed in the scaleless carp support the hypothesis that gill remodeling during hypoxia is a general characteristic of cold water carp species, the reduced magnitude of the response in scaleless carp relative to goldfish and crucian carp may be a reflection of their more active lifestyle or because they reside in a moderately hypoxic environment at altitude.

Original languageEnglish
Pages (from-to)1063-1074
Number of pages12
JournalJournal of Experimental Biology
Volume211
Issue number7
DOIs
StatePublished - Apr 1 2008

Fingerprint

Carps
hypoxia
Lakes
carp
gills
lakes
China
lake
Water
Carassius
surface area
Goldfish
general characteristics
goldfish
mitochondrion
ultrastructure
plasma
cold water
water
Gymnocypris przewalskii

Keywords

  • Gill morphology
  • Hypoxia
  • Ionoregulation
  • Mitochondria rich cell
  • Osmorespiratory compromise

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. / Matey, Victoria; Richards, Jeffrey G.; Wang, Yuxiang; Wood, Chris M.; Rogers, Joe; Davies, Rhiannon; Murray, Brent W.; Chen, X. Q.; Du, Jizeng; Brauner, Colin J.

In: Journal of Experimental Biology, Vol. 211, No. 7, 01.04.2008, p. 1063-1074.

Research output: Contribution to journalArticle

Matey, V, Richards, JG, Wang, Y, Wood, CM, Rogers, J, Davies, R, Murray, BW, Chen, XQ, Du, J & Brauner, CJ 2008, 'The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii', Journal of Experimental Biology, vol. 211, no. 7, pp. 1063-1074. https://doi.org/10.1242/jeb.010181
Matey, Victoria ; Richards, Jeffrey G. ; Wang, Yuxiang ; Wood, Chris M. ; Rogers, Joe ; Davies, Rhiannon ; Murray, Brent W. ; Chen, X. Q. ; Du, Jizeng ; Brauner, Colin J. / The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. In: Journal of Experimental Biology. 2008 ; Vol. 211, No. 7. pp. 1063-1074.
@article{9264d9c42e86465c89509894a1647f28,
title = "The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii",
abstract = "Goldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3 mg O2 l-1) for 24 h followed by 12 h recovery in normoxic water (6 mg O2 l-1 at 3200 m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8 h of hypoxia and almost complete by 24 h, and included a gradual reduction of filament epithelial thickness (>50{\%}), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60{\%}) and reduction in epithelial water-blood diffusion distance (<50{\%}). An increase in caspase 3 activity in gills occurred following 24 h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15{\%} reduction in plasma [Na+] and [Cl-], respectively, within 12-24 h of hypoxia. Within 12 h of hypoxia exposure, 'wavy-convex'-mitochondria rich cells (MRCs) with large apical crypts and numerous branched microvilli were transformed into small 'shallow-basin' cells with a flattened surface. As the apical membrane of MRCs is the site for active ion uptake from the water, a reduction in apical crypt surface area may have contributed to the progressive reduction in plasma [Na+] and [Cl -] observed during hypoxia. The changes in the macro- and ultra-structure of fish gills, and plasma [Na+] and [Cl-] during hypoxia were reversible, showing partial recovery by 12 h following return to normoxia. Although the large morphological changes in the gill observed in the scaleless carp support the hypothesis that gill remodeling during hypoxia is a general characteristic of cold water carp species, the reduced magnitude of the response in scaleless carp relative to goldfish and crucian carp may be a reflection of their more active lifestyle or because they reside in a moderately hypoxic environment at altitude.",
keywords = "Gill morphology, Hypoxia, Ionoregulation, Mitochondria rich cell, Osmorespiratory compromise",
author = "Victoria Matey and Richards, {Jeffrey G.} and Yuxiang Wang and Wood, {Chris M.} and Joe Rogers and Rhiannon Davies and Murray, {Brent W.} and Chen, {X. Q.} and Jizeng Du and Brauner, {Colin J.}",
year = "2008",
month = "4",
day = "1",
doi = "10.1242/jeb.010181",
language = "English",
volume = "211",
pages = "1063--1074",
journal = "Journal of Experimental Biology",
issn = "0022-0949",
publisher = "Company of Biologists Ltd",
number = "7",

}

TY - JOUR

T1 - The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii

AU - Matey, Victoria

AU - Richards, Jeffrey G.

AU - Wang, Yuxiang

AU - Wood, Chris M.

AU - Rogers, Joe

AU - Davies, Rhiannon

AU - Murray, Brent W.

AU - Chen, X. Q.

AU - Du, Jizeng

AU - Brauner, Colin J.

PY - 2008/4/1

Y1 - 2008/4/1

N2 - Goldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3 mg O2 l-1) for 24 h followed by 12 h recovery in normoxic water (6 mg O2 l-1 at 3200 m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8 h of hypoxia and almost complete by 24 h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water-blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24 h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na+] and [Cl-], respectively, within 12-24 h of hypoxia. Within 12 h of hypoxia exposure, 'wavy-convex'-mitochondria rich cells (MRCs) with large apical crypts and numerous branched microvilli were transformed into small 'shallow-basin' cells with a flattened surface. As the apical membrane of MRCs is the site for active ion uptake from the water, a reduction in apical crypt surface area may have contributed to the progressive reduction in plasma [Na+] and [Cl -] observed during hypoxia. The changes in the macro- and ultra-structure of fish gills, and plasma [Na+] and [Cl-] during hypoxia were reversible, showing partial recovery by 12 h following return to normoxia. Although the large morphological changes in the gill observed in the scaleless carp support the hypothesis that gill remodeling during hypoxia is a general characteristic of cold water carp species, the reduced magnitude of the response in scaleless carp relative to goldfish and crucian carp may be a reflection of their more active lifestyle or because they reside in a moderately hypoxic environment at altitude.

AB - Goldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3 mg O2 l-1) for 24 h followed by 12 h recovery in normoxic water (6 mg O2 l-1 at 3200 m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8 h of hypoxia and almost complete by 24 h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water-blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24 h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na+] and [Cl-], respectively, within 12-24 h of hypoxia. Within 12 h of hypoxia exposure, 'wavy-convex'-mitochondria rich cells (MRCs) with large apical crypts and numerous branched microvilli were transformed into small 'shallow-basin' cells with a flattened surface. As the apical membrane of MRCs is the site for active ion uptake from the water, a reduction in apical crypt surface area may have contributed to the progressive reduction in plasma [Na+] and [Cl -] observed during hypoxia. The changes in the macro- and ultra-structure of fish gills, and plasma [Na+] and [Cl-] during hypoxia were reversible, showing partial recovery by 12 h following return to normoxia. Although the large morphological changes in the gill observed in the scaleless carp support the hypothesis that gill remodeling during hypoxia is a general characteristic of cold water carp species, the reduced magnitude of the response in scaleless carp relative to goldfish and crucian carp may be a reflection of their more active lifestyle or because they reside in a moderately hypoxic environment at altitude.

KW - Gill morphology

KW - Hypoxia

KW - Ionoregulation

KW - Mitochondria rich cell

KW - Osmorespiratory compromise

UR - http://www.scopus.com/inward/record.url?scp=43049086695&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=43049086695&partnerID=8YFLogxK

U2 - 10.1242/jeb.010181

DO - 10.1242/jeb.010181

M3 - Article

C2 - 18344480

AN - SCOPUS:43049086695

VL - 211

SP - 1063

EP - 1074

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 7

ER -