Phosphate absorption across multiple epithelia in the Pacific hagfish (Eptatretus stoutii)

Abstract

Inorganic phosphate (Pi) is an essential nutrient for all organisms, but in seawater, Pi is a limiting nutrient. This study investigated the primary mechanisms of Pi uptake in Pacific hagfish ( Eptatretus stoutii) using ex vivo physiological and molecular techniques. Hagfish were observed to have the capacity to absorb Pi from the environment into at least three epithelial surfaces: the intestine, skin, and gill. Pi uptake in all tissues was concentration dependent, and saturable Pi transport was observed in the skin and gill at <2.0 mmol/l Pi. Gill and intestinal Pi uptake was sodium dependent, but Pi uptake into the skin increased under low sodium conditions. Gill Pi transport exhibited an apparent affinity constant ∼0.23–0.6 mmol/l Pi. A complete sequence of a type II sodium phosphate cotransporter (Slc34a) was obtained from the hagfish gill. Phylogenetic analysis of the hagfish Slc34a transporter indicates that it is earlier diverging than, and/or ancestral to, the other identified vertebrate Slc34a transporters (Slc34a1, Slc34a2, and Slc34a3). With the use of RT-PCR, the hagfish Slc34a transcript was detected in the intestine, skin, gill, and kidney, suggesting that this may be the transporter involved in Pi uptake into multiple epithelia in the hagfish. This is the first measurement of Pi uptake across the gill or skin of any vertebrate animal and first sodium phosphate cotransporter identified in hagfish.

Acquisition of alanyl‐alanine in an Agnathan: Characteristics of dipeptide transport across the hindgut of the Pacific hagfish Eptatretus stoutii

“…The rate of L ‐ala‐ala uptake was unaltered along the length of the hindgut. This feature is characteristic of hagfish intestinal nutrient uptake (Glover et al ., ; Schultz et al ., ; Weinrauch et al ., , ) and could conceivably be the result of both feeding behaviour and intestinal morphology. Hagfishes obtain food episodically through both active predation (Zintzen et al ., ) and opportunistic scavenging (Martini, ).…”

“…Indeed, hagfish are capable of acquiring nutrients across multiple epithelia including the skin and gills, much like soft‐bodied marine invertebrates (Glover et al ., ). Although these animals are agastric and have a primitive digestive system consisting of a straight, undifferentiated hindgut (Adam, ; Weinrauch et al ., ), nutrient transport mechanisms appear to be highly conserved relative to those of later‐diverging vertebrates (Glover et al ., , ; Schultz et al ., ; Weinrauch et al ., ; Young et al ., ). These animals are therefore ideally suited for studies aiming to understand the evolution of early vertebrate nutrient transport systems.…”

Hagfish Houdinis: biomechanics and behavior of squeezing through small openings

“…Davison et al (1990) found no evidence that the SCS serves as a sink for lactate ions during exhaustive exercise, and the SCS is also unlikely to serve as a hydrostatic skeleton given its flaccid nature (Forster et al, 1989). Recent studies have demonstrated cutaneous transport of nutrients (Glover et al, 2011;Schultz et al, 2014), ammonia and trace metals (Glover et al, 2015) in Pacific hagfish, suggesting that the large blood volume held within the SCS may be involved in acidbase regulation and nutrient acquisition from the surrounding water. Whatever the function of the SCS, the occurrence of this distensible compartment surrounding the hagfish's body is likely to have implications for locomotion within confined spaces.…”

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

“…Recent studies have highlighted the importance of cutaneous transport in Pacific hagfish (Eptatretus stoutii) for nutrient acquisition (Glover et al, 2011;Schultz et al, 2014), ammonia and base excretion , and trace metal uptake ; however, the role of hagfish skin in O 2 uptake (ṀO 2 ) is contentious. Cutaneous respiration has been demonstrated in the phylogenetically related lamprey (Geotria australis) in larval form (Potter et al, 1996) and the European eel (Anguilla anguilla) (Nonnotte and Kirsch, 1978), both of which share similar body plans to hagfish, as well as in several species of fish such as the inanga (Galaxias maculatus) (Urbina et al, 2012(Urbina et al, , 2014, flounder (Platichthys flesus) and sole (Solea solea) (Nonnotte and Kirsch, 1978).…”