Cellular and epithelial adjustments to altered salinity in the gill and opercular epithelium of a cichlid fish (Oreochromis mossambicus)

Kültz, Dietmar; Jürss, K.; Jonas, Ludwig

doi:10.1007/bf00300692

Cited by 55 publications

(33 citation statements)

References 46 publications

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“…Therefore, it is possible to validate the workflow by assessing how well it reproduces previously established or expected effects on abundances of certain gill proteins. In particular, it is well known that the number and size of gill mitochondriarich ionocytes increase significantly when FW-acclimated Mozambique tilapia are exposed to severe acute (34 ppt) or gradual (90 ppt) salinity stress (8,(41)(42)(43). The extent of increase in mitochondria-rich ionocyte quantity at the cellular level is readily reflected in the extent of increased abundance of mitochondrial proteins under comparable conditions in this study.…”

Section: Discussionsupporting

confidence: 56%

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Quantitative Molecular Phenotyping of Gill Remodeling in a Cichlid Fish Responding to Salinity Stress

Kültz

Gardell

et al. 2013

Molecular & Cellular Proteomics

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A two-tiered label-free quantitative (LFQ) proteomics workflow was used to elucidate how salinity affects the molecular phenotype, i.e. proteome, of gills from a cichlid fish, the euryhaline tilapia (Oreochromis mossambicus). The workflow consists of initial global profiling of relative tryptic peptide abundances in treated versus control samples followed by targeted identification (by MS/MS) and quantitation (by chromatographic peak area integration) of validated peptides for each protein of interest. Fresh water acclimated tilapia were independently exposed in separate experiments to acute short-term (34 ppt) and gradual long-term (70 ppt, 90 ppt) salinity stress followed by molecular phenotyping of the gill proteome. The severity of salinity stress can be deduced with high technical reproducibility from the initial global label-free quantitative profiling step alone at both peptide and protein levels. However, an accurate regulation ratio can only be determined by targeted label-free quantitative profiling because not all peptides used for protein identification are also valid for quantitation. Of the three salinity challenges, gradual acclimation to 90 ppt has the most pronounced effect on gill molecular phenotype. Known salinity effects on tilapia gills, including an increase in the size and number of mitochondria-rich ionocytes, activities of specific ion transporters, and induction of specific molecular chaperones are reflected in the regulation of abundances of the corresponding proteins. Moreover, specific protein isoforms that are responsive to environmental salinity change are resolved and it is revealed that salinity effects on the mitochondrial proteome are nonuniform. Furthermore, protein NDRG1 has been identified as a novel key component of molecular phenotype restructuring during salinity-induced gill remodeling. In conclusion, besides confirming known effects of salinity on gills of euryhaline fish, molecular phenotyping reveals novel insight into proteome changes that underlie the remodeling of tilapia gill epithelium in response to environmental salinity change. Molecular & Cellular Proteomics 12: 10.1074/ mcp.M113.029827, 3962-3975, 2013.Euryhaline fish are capable of living in fresh water (FW), 1 brackish water (BW), seawater (SW), and hypersaline water (ϾSW). They adjust transepithelial ion transport across gill epithelium when challenged by an environmental salinity change (1). Acclimation from hyposmotic (relative to plasma, e.g. FW) to hyperosmotic (relative to plasma, e.g. SW) environments is accompanied by extensive remodeling of gill epithelium, the most prominent feature of which is an increase in the number and size of salt-secretory, mitochondria-rich ionocytes (2). In addition, molecular chaperones and distinct sets of transport proteins are activated when euryhaline fish are challenged by increasing environmental salinity (3)(4)(5). A euryhaline fish species in which these physiological responses have been observed is the Mozambique tilapia, Oreochromis mossambicus (6 -8). Tilapi...

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Section: Discussionsupporting

confidence: 56%

“…This species and tissue were chosen because considerable prior knowledge on gill responses to salinity stress exists (4,8,13,17). Therefore, it is possible to validate the workflow by assessing how well it reproduces previously established or expected effects on abundances of certain gill proteins.…”

Section: Discussionmentioning

confidence: 99%

Quantitative Molecular Phenotyping of Gill Remodeling in a Cichlid Fish Responding to Salinity Stress

Kültz

Gardell

et al. 2013

Molecular & Cellular Proteomics

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“…and Cl -taken up must be excreted across the branchial epithelium. Since MRCs are the primary branchial cells responsible for the transport of monovalent ions, a proliferation of these cells on the gills of fish in hyper-saline waters could be expected, and in fact, studies on tilapia have shown an increase in branchial MRC density and/or size relative to fish in seawater (Kultz and Onken 1993;Kultz et al 1995;Uchida et al 2000;Ouattara et al 2009). Together these two changes represent an increased functional surface area that is usually ascribed to greater transport capacity.…”

Section: Physiology Of Hyper-saline Tolerant Fishmentioning

confidence: 97%

The physiology of hyper-salinity tolerance in teleost fish: a review

Gonzalez

2011

J Comp Physiol B

109

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Hyper-saline habitats (waters with salinity >35 ppt) are among the harshest aquatic environments. Relatively few species of teleost fish can tolerate salinities much above 50 ppt, because of the challenges to osmoregulation, but those that do, usually estuarine, euryhaline species, show a strong ability to osmoregulate in salinities well over 100 ppt. Typically, plasma Na(+) and Cl(-) concentrations rise slowly or not at all up to about 65 ppt. At higher salinities ion levels do rise, but the increase is small relative to the magnitude of increase in concentrations of the surrounding water. A number of adjustments are responsible for such strong osmoregulation. Reduced branchial water permeability is indicated by the observation that with the exposure to hyper-salinities drinking rates rise more slowly than the branchial osmotic gradient. Lower water permeability limits osmotic water loss and greatly reduces the salt load incurred in replacing it. Still, increased gut Na(+)/K(+)-ATPase (NAK) activity is necessary to absorb the larger gut salt load and increased HCO(3) (-) secretion is required to precipitate Ca(2+) and some Mg(2+) in the imbibed water to facilitate water absorption. All Na(+) and Cl(-) taken up must be excreted and increased branchial salt excreting capacity is indicated by elevated mitochondrion-rich cell density and size, gill NAK activity and expression of chloride channels. Excretion of Na(+) and Cl(-) occurs against a larger gradient than in seawater and calculation of the equilibrium potential for Na(+) across the gill epithelium indicates that the trans-epithelial potential required for excretion of Na(+) climbs with salinity up to about 65 ppt before leveling off due to the increasing plasma Na(+) levels. During acute transition to SW or mildly hyper-saline waters, some species have shown the ability to upregulate branchial NAK activity rapidly and this may play an important role in limiting disturbances at higher salinities. It does not appear that the opercular epithelium, which in SW acts in a way that is functionally similar to the gills, continues to do so in hyper-saline waters. Little is know about the hormones involved in acclimation to hyper-salinity, but the few studies available suggest a role for cortisol, but not growth hormone and insulin-like growth factor. Despite the increased transport capacity evident in both the gill and gut in hyper-saline waters there is no clear trend toward increased metabolic rate. These studies provide a general outline of the mechanisms of osmoregulation in these species, but significant questions still remain.

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“…La description et la quantification des cellules à chlorures fonctionnelles ont été menées chez de nombreuses espèces euryhalines telles que le tilapia Oreochromis mossambicus (Kültz et al, 1995, Lee et al, 2003, le tilapia hybride d'Oreochromis mossambicus x Oreochromis urolepis hornorum (Sarsella et al, 2004). Bien qu'il existe des différences dans l'anatomie générale des branchies entre les différents groupes de poissons, les cellules qui composent l'épithélium branchial sont très similaires (Wilson et Laurent, 2002).…”

Section: Discussionunclassified

Influence de la salinité sur la structure des branchies et l’ultrastructure des ionocytes Chez le tilapia <i>Sarotherodon melanotheron heudelotii</i> provenant d'un estuaire hypersalé (Saloum, Sénégal).

Ouattara¹,

Ouattara²,

Bamba³

et al. 2014

J. App. Bioscience.

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Ouattara et al. J. Appl. Biosci. 2014. Influence de la salinité sur la structure des branchies et l'ultrastructure des ionocytes chez le tilapia provenant d'un estuaire hypersalé (Sénégal). 6808Influence de la salinité sur la structure des branchies et l'ultrastructure des ionocytes Chez le tilapia Sarotherodon melanotheron heudelotii provenant d'un estuaire hypersalé (Saloum, Sénégal). 6809ABSTRACT Objective: This study describes the structure of gills and the ultrastructural changes in gill ionocytes of the tilapia S. m. heudelotii from a hypersaline estuary (Saloum, Senegal), subject to variations in salinity of 0,3; 35; 70 and 90‰ in laboratory for 72 h. Methodology and Results: Juvenile S. m. heudelotii were subjected to concentrations of salinity ranging from freshwater (0,3‰) to hypersaline water (90‰). The gills structure and the location of ionocytes were studied by photonic histology and ionocytes ultratrastructure described by transmission electronic microscopy. Four gill arches were identified. At 0,3‰ of salinity, ionocytes were observed at the base of filaments, while at 35‰ and more, they have been examined on the filaments and lamellae. Three types of ionocytes were identified according to the composition of the cytoplasm and two types according to the opening of the apical crypt. Conclusion and Application: This study shows for the first time that tilapia s. m. Heudelotii adapts to changes in concentration of salinity by modification of the location and ultrastructure of its gill ionocytes. These results suggested that this species can also fit perfectly into the high salinity, that other tilapia do not support, for example Oreochromis niloticus. It might therefore serve as a biological model in the perspective of a fish farming in brackish water or seawater. Indeed, tilapia culture is carried out mainly in fresh water that is keenly competed for direct consumption by human people and for industrial uses. However, marine and lagoon ecosystems have enormous fish farming potential, but very less exploited. Furthermore, these results may help to understand the phenomena of speciation in some species associated with the environmental disruption caused by climate change.

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Cellular and epithelial adjustments to altered salinity in the gill and opercular epithelium of a cichlid fish (Oreochromis mossambicus)

Cited by 55 publications

References 46 publications

Quantitative Molecular Phenotyping of Gill Remodeling in a Cichlid Fish Responding to Salinity Stress

Quantitative Molecular Phenotyping of Gill Remodeling in a Cichlid Fish Responding to Salinity Stress

The physiology of hyper-salinity tolerance in teleost fish: a review

Influence de la salinité sur la structure des branchies et l’ultrastructure des ionocytes Chez le tilapia <i>Sarotherodon melanotheron heudelotii</i> provenant d'un estuaire hypersalé (Saloum, Sénégal).

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