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Osmoregulation and Excretion Erik Hviid Larsen,*1 Lewis E

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Osmoregulation and Excretion Erik Hviid Larsen,*1 Lewis E Osmoregulation and Excretion Erik Hviid Larsen,*1 Lewis E. Deaton,2 Horst Onken,3 Michael O’Donnell,4 Martin Grosell,5 William H. Dantzler,6 and Dirk Weihrauch7 ABSTRACT The article discusses advances in osmoregulation and excretion with emphasis on how multicellu- lar animals in different osmotic environments regulate their milieu interieur´ . Mechanisms of energy transformations in animal osmoregulation are dealt with in biophysical terms with respect to wa- ter and ion exchange across biological membranes and coupling of ion and water fluxes across epithelia. The discussion of functions is based on a comparative approach analyzing mechanisms that have evolved in different taxonomic groups at biochemical, cellular and tissue levels and their integration in maintaining whole body water and ion homeostasis. The focus is on recent studies of adaptations and newly discovered mechanisms of acclimatization during transitions of animals between different osmotic environments. Special attention is paid to hypotheses about the diversity of cellular organization of osmoregulatory and excretory organs such as glomerular kidneys, antennal glands, Malpighian tubules and insect gut, gills, integument and intestine, with accounts on experimental approaches and methods applied in the studies. It is demonstrated how knowledge in these areas of comparative physiology has expanded considerably during the last two decades, bridging seminal classical works with studies based on new approaches at all levels of anatomical and functional organization. A number of as yet partially unanswered questions are emphasized, some of which are about how water and solute exchange mechanisms at lower levels are integrated for regulating whole body extracellular water volume and ion homeostasis C of animals in their natural habitats. ⃝ 2014 American Physiological Society. Compr Physiol 4:405-573, 2014. Introduction The ideas of the above seminal works are embedded in the comparative physiology of osmoregulation and excretion In his lecture series as professor of comparative physiology dealing with the regulation of composition and volume of the at the Museum of Natural History in Paris Claude Bernard internal milieu of multicellular organisms exposed to differ- (1813-1878) wrote: “I believe I was the first to insist on the ent and time-varying external milieus. In order to study the concept that animals have actually two milieus; an external regulation of fluxes of solutes and water between the animal milieu in which the organism is located and an internal milieu and the surroundings, the transport systems and their energy in which the elements of its tissues live. The real existence requirement have to be identified and related to the anatom- of a living thing does not take place in the external milieu, ical and cellular organization of ion- and water-transporting which is the atmosphere for air breathing creatures and fresh tissues and excretory organs, which have constituted major or salt water for aquatic animals, but in the liquid internal efforts in comparative studies of osmoregulation and milieu formed by the circulating organic fluid surrounding excretion. and bathing all the anatomical elements of the tissue” (113). Inspired by this idea of Bernard and his own studies of glucose metabolism, body temperature and acid-base balance, Walter *Correspondence to [email protected] B. Cannon (1871-1945) developed the concept of “homeosta- 1Department of Biology, the August Krogh Centre, University of Copenhagen, Copenhagen, Denmark sis.” Homeostasis, Cannon pointed out, would require mech- 2Biology Department, University of Louisiana at Lafayette, Lafayette, anisms operating simultaneously or successively in such a Louisiana way that perturbation of a physiological variable initiates pro- 3Department of Biological Sciences, Wagner College, Staten Island, cesses that would counter the change (250). In experiments New York with freshwater animals, August Krogh (1874-1949) discov- 4Department of Biology, McMaster University, Hamilton, Ontario, Canada ered that their osmoregulation depends on active ion transport 5RSMAS, University of Miami, Miami, Forida across the skin and gills and concluded that the different ion 6Department of Physiology, University of Arizona, Tucson, Arizona composition of the extracellular and intracellular body fluids, 7Department of Biological Sciences, University of Manitoba, and of freshwater animals and their natural surroundings, “has Winnipeg, Manitoba, Canada not to do with a true equilibrium, but with a steady state main- Published online, April 2014 (comprehensivephysiology.com) tained against a passive diffusion and requiring expenditure DOI: 10.1002/cphy.c130004 of energy” (974). Copyright C American Physiological Society. ⃝ Volume 4, April 2014 405 Osmoregulation and Excretion Comprehensive Physiology 18 The present article is organized as follows. The initial sec- H2O ,orbyacombinationofthetracertechniquefordeter- tion on “Biophysical Concepts in Osmoregulation” presents mining one of the unidirectional fluxes and a volumetric mea- commonly used concepts and theoretical tools for the study surement of the net flux of water. Water transport across bio- of water and ion exchange in animals. Some mathematics is logical membranes takes place in the lipid bilayer between necessary in order to express the issue in a precisely defined integral proteins (532), via aquaporins constituting selective form. This is done here by explaining the results in qualitative, water-permeable pores (7, 8, 1483, 1484), and in the narrow biologically relevant terms of importance for animal osmoreg- tight junctions of the paracellular pathway of absorbing and ulation. The subsequent sections are organized according to secreting epithelia (906, 1892, 1984). Although the transport taxonomic groups to emphasize that comparative physiology is passive, Eq. (1a) is rarely obeyed because bulk water flow of osmoregulation is about principles and diversity of adap- in pores violates the assumption of random thermal move- tations that have evolved among different animal species to ment of individual water molecules, which was discovered cope with changing osmotic environments. Our discussions already in the early studies of water transport in biological include physiological and biochemical mechanisms at all lev- systems (746, 955, 1399). Since then, it has been a major els of functional organization. It will be clear that scientific challenge for physiologists to develop a consistent theoretical progress in different taxa proceeds along somewhat different framework for handling of water transport across biological paths. We aim at a review on the experimental background of membranes (532, 804). the present ideas and at providing stepping-stones for future The chemical potential of water is determined by the mole studies of this major and expanding field of comparative phys- fraction of water (Xw)accordingto(1761), iology. Specifically, the future challenge is to integrate whole O body, isolated tissue, and cell physiological research with µw µw (T, p) RT ln Xw progress in studies on the organization of the genome and = + O expression patterns. where µw (T, p)isthechemicalpotentialofpurewater (Xw 1) at temperature, T,andpressure,p.Assumethat compartment= (a)containspurewaterandisseparatedfrom compartment (b)ofsimilartemperature,butcontainingthe Biophysical Concepts impermeable solute, s of mole fraction Xs.Thus,Xw 1 = in Osmoregulation of compartment (a), and Xw Xs 1ofcompartment(b). + = (a) (b) Thermodynamic equilibrium for water, µw µw , requires, The section summarizes quantitative treatments of water and = ion transport across plasma membranes and epithelia, which O (a) O (b) µw (T, p ) µw (T, p ) RT ln Xw are pertinent to studies and discussions of animal osmoregu- = + lation. (b) (a) Since Xw < 1, RTlnXw is negative. Thus, p p > 1, which is the osmotic pressure, !,ofthesolutionincompartment(− b) given by the following thermodynamically exact expression Chemical Potential of Water, Osmotic Pressure, (1761), and the van’t Hoff Equation RT Assume two compartments of water, (a)and(b), separated ! ln(1 Xs )(2) by a water-permeable membrane. The chemical potentials of =− V w − (a) (b) water are given the symbols, µw andµw . If water is not in ! " (a) (b) where V is the mean value of the molar water volume, V , thermodynamic equilibrium (µw µw ), there is a (net) flux w w ̸= (a) (b) of water, J (net),directedfromthecompartmentofthehigher in the pressure range p to p .Foradilutesolution,Xs 1 w ! " ≪ chemical potential to that of the lower chemical potential. If and ln(1 Xs) Xs that leads to, − ≈− there is no interaction in the membrane between the water molecules or between water molecules and other moving par- RT ! Xs (3a) ticles, the flux-ratio equation applies (1889), = V w Introducing the concentration! of" the solute rather than its (a) (b) Jw → (a) (b) mole fraction presupposes further mathematical approxima- RT ln (a) (b) µw µw (1a) Jw ← = − tions. Since Eq. (3a) assumes the solution to be dilute, (net) (a) (b) (a) (b) X n /(n n ) n /n ,wheren and n are the num- Jw Jw → Jw ← (1b) s s w s s w s w = − ber= of gram molecules+ ≈ of s and w.Thus, 1 1 where R is the universal gas constant (8.31 J K− mol− or RT 1 1 · · ! ns 0.082 l atm K− mol− )andT the absolute temperature (K). = · · · (a) (b) (a) (b) nw V w (3b) The unidirectional water fluxes (Jw → , Jw ← )aremea- ns 3 RT! " sured by the isotope tracer technique using H2O, D2O or = [Vw] 406 Volume 4, April 2014 Comprehensive
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