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Osmoregulation in the Hawaiian Anchialine Shrimp Halocaridina Rubra

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Osmoregulation in the Hawaiian Anchialine Shrimp Halocaridina Rubra © 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 2309-2320 doi:10.1242/jeb.103051 RESEARCH ARTICLE Osmoregulation in the Hawaiian anchialine shrimp Halocaridina rubra (Crustacea: Atyidae): expression of ion transporters, mitochondria-rich cell proliferation and hemolymph osmolality during salinity transfers Justin C. Havird1,2,*, Scott R. Santos1,2 and Raymond P. Henry1 ABSTRACT environment when in dilute seawater (SW) (reviewed by Mantel and Studies of euryhaline crustaceans have identified conserved Farmer, 1983) through active salt transport across the gills (reviewed osmoregulatory adaptions allowing hyper-osmoregulation in dilute by Péqueux, 1995; Charmantier et al., 2009; Henry et al., 2012; waters. However, previous studies have mainly examined decapod McNamara and Faria, 2012). In SW, the overwhelming majority of brachyurans with marine ancestries inhabiting estuaries or tidal marine crustaceans act as osmoconformers, with internal creeks on a seasonal basis. Here, we describe osmoregulation in the hemolymph osmolality mirroring concentrations in the ambient atyid Halocaridina rubra, an endemic Hawaiian shrimp of freshwater medium (Henry, 2001; Henry et al., 2012). However, during transfer ancestry from the islands’ anchialine ecosystem (coastal ponds with to water below ~26‰, hyper-osmoregulatory mechanisms are subsurface freshwater and seawater connections) that encounters activated in euryhaline crustaceans (Henry, 2005). This near-continuous spatial and temporal salinity changes. Given this, physiological transition enables survival in the fluctuating salinity survival and osmoregulatory responses were examined over a wide of environments such as estuaries, allowing euryhaline species to salinity range. In the laboratory, H. rubra tolerated salinities of take advantage of these highly productive environments (Gross, ~0–56‰, acting as both a hyper- and hypo-osmoregulator and 1972) without competition from stenohaline species. Although some −1 maintaining a maximum osmotic gradient of ~868 mOsm kg H2O in marine osmoconformers can survive in salinities as low as ~10‰, freshwater. Furthermore, hemolymph osmolality was more stable their lower limit is typically in the range 16–18‰ (Kinne, 1971; during salinity transfers relative to other crustaceans. Silver nitrate Hsueh et al., 1993). Thus, only osmotic/ionic regulators are capable and vital mitochondria-rich cell staining suggest all gills are of traversing wide salinity ranges like those spanning from SW osmoregulatory, with a large proportion of each individual gill (35‰) to freshwater (FW; near 0‰). functioning in ion transport (including when H. rubra acts as an Osmoregulation in brachyuran crabs takes place in the osmoconformer in seawater). Additionally, expression of ion mitochondria-rich cells (MRCs) of the posterior gills, which are transporters and supporting enzymes that typically undergo characterized by a thick (10–20 μm) osmoregulatory epithelium, in upregulation during salinity transfer in osmoregulatory gills (i.e. contrast to the anterior gills, which are characterized by a thin Na+/K+-ATPase, carbonic anhydrase, Na+/K+/2Cl– cotransporter, V- (1–2 μm) respiratory epithelium (Taylor and Taylor, 1992; Freire et type H+-ATPase and arginine kinase) were generally unaltered in H. al., 2008). However, all gills in crayfishes and shrimps possess rubra during similar transfers. These results suggest H. rubra (and MRCs and are involved in osmoregulation, although some areas of possibly other anchialine species) maintains high, constitutive levels individual gills remain specialized for respiration (Wheatly and of gene expression and ion transport capability in the gills as a means Henry, 1987; Dickson et al., 1991; McNamara and Lima, 1997; of potentially coping with the fluctuating salinities that are Ordiano et al., 2005; Huong et al., 2010). Active salt absorption in encountered in anchialine habitats. Thus, anchialine taxa represent the MRCs is accomplished via a suite of ion transporters and an interesting avenue for future physiological research. supporting enzymes (Evans et al., 2005; Henry et al., 2012): in this context, Na+ absorption occurs via a combination of apical Na+/H+ KEY WORDS: Arginine kinase, Carbonic anhydrase, Crustacean, exchange, Na+/K+/2Cl– co-transport, Na+ channels and the + + + + – Euryhaline, Gene expression, Gill, Na /K -ATPase, Na /K /2Cl basolateral Na+/K+-ATPase (NKA), while Cl– absorption is co-transporter, qPCR, Salt/ion transport, Transcriptome, V-type – – accomplished via apical co-transport, Cl /HCO3 exchange and + H -ATPase basolateral Cl– channels (reviewed in Freire et al., 2008; Charmantier et al., 2009; Henry et al., 2012; McNamara and Faria, INTRODUCTION 2012). Of these, NKA, which establishes the required Euryhaline crustaceans can function as strong osmoregulators that electrochemical gradient for ion transport into the hemolymph, and maintain internal osmotic concentrations above those of the external cytoplasmic carbonic anhydrase (CA), which produces H+ and – + + – – HCO3 needed to support Na /H and Cl /HCO3 exchange, have been extensively studied during salinity acclimation in crustaceans 1 Department of Biological Sciences and Cellular and Molecular Biosciences (e.g. Towle et al., 1976; Henry and Cameron, 1982a; Towle and Program, Auburn University, Auburn, AL 36849, USA. 2Molette Biology Laboratory for Environmental and Climate Change Studies, Auburn University, Auburn, Kays, 1986; Henry, 2001). Overall, these enzymes generally have AL 36849, USA. higher activities: (1) in euryhaline versus stenohaline crustaceans (Henry, 1984; Harris and Bayliss, 1988) (but see Piller et al., 1995), *Author for correspondence ([email protected]) (2) in gills versus other tissues (e.g. Henry, 2001; Lucu and Flik, Received 27 January 2014; Accepted 31 March 2014 1999), (3) in osmoregulatory versus respiratory gills (Henry, 1984; The Journal of Experimental Biology 2309 RESEARCH ARTICLE The Journal of Experimental Biology (2014) doi:10.1242/jeb.103051 and Henry, 1987). FW species also tend to be weaker hyper- List of symbols and abbreviations osmoregulators in FW, maintaining a hemolymph osmolality at AK arginine kinase ~370–450 mOsm above ambient medium (Mantel and Farmer, 1983) BB Baby Bear compared with ~600 mOsm in species such as C. sapidus and BH Blue Hole CA(c/g) carbonic anhydrase (c or g isoform) Eriocheir sinensis (Cameron, 1978; Onken, 1999). Ct threshold cycle The majority of osmoregulatory studies have focused on DASPMI 4-[4-(dimethylamino)styryl]-N-methylpyridinium iodide euryhaline crustaceans with marine ancestry that only spend part of EP Eric’s Pond their life cycle in dilute SW or FW. Given this, extending such FW freshwater studies to other taxonomic or ecological groups could provide + HAT V-type H -ATPase further insight into the evolution of osmoregulatory mechanisms. HM Cape Hanamanioa ICP-OES inductively coupled plasma optical emission spectrometry For example, studies utilizing the FW caridean genus IH Issac Hale Macrobrachium have revealed mechanisms that contrast with those JP Joe’s Pond in brachyuran crabs (McNamara and Lima, 1997; Ordiano et al., KBP Kalaeloa Unit 2005; Huong et al., 2010). Crustaceans from the anchialine KIKI Keawaiki Bay ecosystem represent another interesting opportunity to do so, as this KONA Kona Coast ecosystem consists of coastal caves and ponds lacking surface MAKA3 Makalawena 3 connections to the open ocean, but which are influenced by both SW MIKE Mike’s Pond MRCs mitochondria-rich cells and FW through underground connections (Holthuis, 1973; Sket, NKA Na+/K+-ATPase 1996). Accordingly, organisms from these habitats can experience NKCC Na+/K+/2Cl– cotransporter daily fluctuations in salinity comparable to those in estuaries due to OWAI Waianae Boat Harbor tides (e.g. 20‰ over 24 hours; Maciolek, 1986). While anchialine PB Papa Bear habitats have a worldwide distribution, they are most concentrated PUHO3A Pu’uhonua o Hōnaunau National Historical Park 3A in the Hawaiian Islands, with ~600 of the ~1000 known anchialine RES1 Restoration 1 SKIP Skippy’s Pond habitats found there (Maciolek and Brock, 1974; Brock, 1987; SW seawater Brock et al., 1987). The most common and abundant macro- TAP Tap’s Pond organism of the Hawaiian anchialine ecosystem is the small (~10 mm), endemic shrimp Halocaridina rubra Holthuis 1963 Holliday, 1985; Böttcher et al., 1990), and (4) during transfers from (Decapoda, Atyidae). This species is found in salinities ranging from high to low salinities (but confined to the osmoregulatory gills) 2–36‰ (Maciolek, 1983) and can be acclimated to salinities ranging (Henry and Watts, 2001; Henry et al., 2002; Henry et al., 2003; from ~0–50‰ in the laboratory (Holthuis, 1973; Maciolek, 1983). Henry, 2005; Roy et al., 2007; Torres et al., 2007; Lucu et al., 2008). Moreover, the family Atyidae has a decisively FW ancestry as: (1) During low-salinity transfers, the need for increased ion transport FW deposits of atyids date to the Cretaceous (Glaessner, 1969; drives MRC proliferation and associated processes in the Smith and Williams, 1981); (2) no extant marine atyids are known osmoregulatory gill lamellae (Neufeld et al., 1980; Lovett et al., (Fryer, 1977), and (3) while some species require salt or brackish 2006). water for larval development (Hunte, 1979a; Hunte, 1979b), most The expression of osmoregulatory genes usually increases in the adult atyids outside the ‘anchialine clade’ are intolerant of SW
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