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Annals of Aquaculture and Research

Lung-Kidney Dual Functions of Fish Gill

Short Communication | Open Access

  • 1. Department of Aquatic Animal Medicine, Huazhong Agricultural University, China
  • 2. Hubei collaborative Innovation Center for Freshwater Aquaculture, People’s Republic of China
  • 3. Key Lab of Freshwater Animal Breeding, Ministry of Agriculture, People’s Republic of China
  • 4. State Key Laboratory of Agricultural Microbiology, People’s Republic of China
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Corresponding Authors
Li Lin, Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, People’s Republic of China, Tel: +86-27-87282113; Fax: +86-27- 87282114
Abstract

Substantial published evidence supports the notion that besides the O2 /CO2 exchange, gill is also a dominant site of ammonia excretion of fish. Therefore, fish gill plays lung-kidney dual functions of human beings. Comparison of traditional Chinese medicine and fish medicine shows that fish gill occupies “ Metal” and “Water” elements which are generating interaction relationship in the “Wu-xing ring”, indicating that the dual functions are closely related. The dual functions are also supported by the observations that many diseases associated with gill normally cause pulmonary-renal syndromes of fish.

Citation

Lin L, Wang W (2014) Lung-Kidney Dual Functions of Fish Gill. Ann Aquac Res 1(1): 1003.

Keywords

•    Fish
•    Gill
•    Function
•    Chinese medicine
•    Fish medicine
•    Wu-xing ring

INTRODUCTION

“ You made him ruler over the works of your hands; You put everything under his feet: all flocks and herds, and the beasts of the field, the birds of the air, and the fish of the sea, all that swim the paths of the seas.” Psalm 8: 6-8.

Fish constitutes an important source of animal protein for the world’s population. World fish food supply has grown dramatically in the last five decades, with an average growth rate of 3.2 percent per year outpacing the increase of 1.7 percent per year in the world’s population. Capture fisheries and aquaculture are two sources of fish products. If we look over the last decade, capture fisheries has been essentially flat. In fact, overfishing has put seafood resources at risk. The United Nations FAO estimates that the world’s major fishing areas and fish species are in decline and in need of urgent management. By contrast, the growth rate of worldwide aquaculture has been sustained and rapid, averaging about 8 percent per year for over thirty years. Therefore, aquaculture has become the major source for fish food supply.

With the rapid progress in aquaculture, new infectious diseases are emerging and becoming the major factors that are hindering the development of fish industry worldwide. Obviously, just like human beings, fish also suffer from diseases. We then ask, are there any parallels between human medicine and fish medicine? In this perspective, we will focus on the functions of fish gill and analyze its position basing on the “Wu-xing” (also named the Five-elements) which is the basis of traditional Chinese medicine. The doctrines of Chinese medicine are rooted in cosmological notions like Yin-yang and Wu-xing. The Wu-xing is a fivefold conceptual scheme that traditional Chinese medicine uses to explain a wide array of phenomena, from the interactions between internal organs to the occurrence of human diseases. The “Five elements” and corresponding five organs are Wood (liver), Fire (heart), Earth (spleen), Metal (lung), and Water (kidney). The “Wu-xing ring” describes two cycles, a generating cycle and an overcoming cycle (Figure 1). In the generating cycle, the order is Wood-Fire-Earth-Metal-Water, which means Wood feeds Fire, Fire creates Earth, Earth bears Metal, Metal enriches Water, and Water nourishes Wood. In the overcoming cycle, the order is Wood-Earth-Water-Fire-Metal, which means Wood parts Earth, Earth dams Water, Water extinguishes Fire, Fire melts Metal, and Metal chops Wood. The “Wu-xing ring” has been being used for describing human diseases in traditional Chinese medicine for more than 2000 years. In general, disease is perceived as a disharmony in the interactions of the five elements (organs) and the interactions between the human body and the environment. We then ask, can we also use the “Wu-xing ring” to describe fish organs and diseases? It is easily to locate the fish liver, heart, spleen and kidney in the “Wu-xing ring”. However, there is no lung instead of gill in fish. We all have known, O2 /CO2 exchange is the most immediately critical function of fish gill, therefore it is easy to place gill at the lung position in the “Wu-xing ring”. In this perspective, we will discuss the kidney function of fish gill. The kidney function of gill was firstly observed by Homer Smith 80 years ago when he demonstrated that freshwater fish excreted their nitrogen waste predominantly as ammonia through the gill [1]. Ever since then, this unexpected phenomenon whetted the appetite of fish biologists and the mechanism of ammonia excretion across fish gill has been intensively investigated. Circumstantial evidence supports the notion that although fish do have kidneys, the gill actually performs most of the renal functions. Molecular techniques have brought new insights into the mechanisms of gill-kidney functions. The human Rhesus protein has been long known to link to the human blood type [2], however, the role of Rh proteins in ammonia transport in erythrocytes has only recently been discovered [3,4]. Furthermore, Rh homologs have been widely observed in yeast [5], bacteria, nematode [6], fish gill, etc. and function as ammonia-transporters [7,8]. There are three Rh homologs in fish, named Rhag, Rhbg, and Rhcg. Rhag occurs in red blood cells, whereas Rhbg and Rhcg localize in basolateral and apical membranes of the branchial epithelium, respectively. Based on the substantial new data available [9-12], including the X-ray crystal structure of Rh proteins [13,14], Patricia A. Wright and Chris M. Wood proposed a “ Na+ /NH4+ exchange metabolon” model to explain branchial ammonia excretion [15]. Briefly, Rhag facilitates NH3 flux out of the erythrocyte, Rhbg moves it across the basolateral membrane of the branchial ionocyte, and Rhcg working together with several membrane transporters ( such as V-type H+ -ATPase, Na+ channel, etc.) as a metabolon for NH4+ excretion [16,17]. Apparently, besides the dominant site for O2 / CO2 exchange, unlike the lung of human beings, gill is also a major site of ammonia excretion, plays critical roles in osmotic and ionic regulation. Fish gill plays a central role in physiological responses to the environment and diseases occurrence.

Taken together, fish gill plays lung-kidney dual functions and occupies two elements (Metal and Water) in the “Wu-xing ring” (Figure 1). Basing on the ring, “Metal enriches Water” which is generating interaction relationship, indicating that the lungkidney dual functions of gill are closely related. In fact, the fish diseases associated with the gill normally result in pulmonaryrenal syndromes which have been widely observed in fish pathological examinations [18]. This observation will shed new light on the diagnosis and treatment of fish diseases.

Acknowledgment

We are thankful to Prof. Dr. Peter Edwards at the Asian Institute of Technology in Thailand for helpful comments. This work was jointly supported by the Fundamental Research Funds for the Central Universities (52204-12020, 2013PY069, 2014PY035) and Natural Science Foundation of China (31372563).

References

1. Smith HW. The excretion of ammonia and urea by the gills of fishes. J Biol Chem. 1929; 81: 727-742.

2. Levine P, Stetson RE. An unusual case of intra group agglutination. J am Med Assoc. 1939; 113: 126-127.

3. Huang CH, Liu Z, Apoil PA,Blancher A. Sequence, organization and evolution of Rh glycoprotein genes in nonhuman primates. J Mol Evol. 2000; 51: 76-87.

4. Avent ND, Reid ME. The Rh blood group system: a review. Blood. 2000; 95: 375-387.

5. Marini AM, Vissers S, Urrestarazu A, André B. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J. 1994; 13: 3456-3463.

6. Huang CH, Peng J. Evolutionary conservation and diversification of Rh family genes and proteins. Proc Natl Acad Sci U S A. 2005; 102: 15512- 15517.

7. Nakada T, Westhoff CM, Kato A, Hirose S. Ammonia secretion from fish gill depends on a set of Rh glycoproteins. FASEB J. 2007; 21: 1067- 1074.

8. Nawata CM, Wood CM. The effects of CO2 and external buffering on ammonia excretion and Rhesus glycoprotein mRNA expression in rainbow trout. J Exp Biol. 2008; 211: 3226-3236.

9. Lin H, Randall DJ. Evidence for the presence of an electrogenic pump on the trout gill epithelium. J Exp Biol. 1991; 161: 119-134.

10. Nawata CM, Wood CM. The effects of CO2 and external buffering on ammonia excretion and Rhesus glycoprotein mRNA expression in rainbow trout. J Exp Biol. 2008; 211: 3226-3236.

11. Tsui TK, Hung CY, Nawata CM, Wilson JM, Wright PA, Wood CM. Ammonia transport in cultured gill epithelium of freshwater rainbow trout: the importance of Rhesus glycoproteins and the presence of an apical Na+/NH4+ exchange complex. J Exp Biol. 2009; 212: 878-892.

12. Braun MH, Steele SL, Ekker M, Perry SF. Nitrogen excretion in developing zebrafish (Danio rerio): a role for Rh proteins and urea transporters. Am J Physiol Renal Physiol. 2009; 296: F994-994F1005.

13. Khademi S, O’Connell J 3rd, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM. Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science. 2004; 305: 1587-1594.

14. Knepper MA, Agre P. Structural biology. The atomic architecture of a gas channel. Science. 2004; 305: 1573-1574.

15. Wright PA, Wood CM. A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol. 2009; 212: 2303-2312.

16. Lin TY, Liao BK, Horng JL, Yan JJ, Hsiao CD, Hwang PP. Carbonic anhydrase 2-like a and 15a are involved in acid-base regulation and Na+ uptake in zebrafish H+-ATPase-rich cells. Am J Physiol Cell Physiol. 2008; 294: C1250-1260.

17. Wood CM, Nawata CM, Wilson JM, Laurent P, Chevalier C, Bergman HL, et al. Rh proteins and NH4(+)-activated Na+-ATPase in the Magadi tilapia (Alcolapia grahami), a 100% ureotelic teleost fish. J Exp Biol. 2013; 216: 2998-3007.

18. Ronald J Roberts. Fish pathology. 4th edn. Wiley-Blackwell Press. 2012; P1-590.

Received : 07 Apr 2014
Accepted : 07 Jun 2014
Published : 09 Jun 2014
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