PHYSIOLOGY OF A BASAL VERTEBRATE, THE SEA LAMPREY (PETROMYZON MARINUS): OSMOREGULATION AND CORTICOSTEROID ACTION

Author

Ciaran A. S. Shaughnessy, University of Massachusetts AmherstFollow

Author ORCID Identifier

https://orcid.org/0000-0003-2146-9126

AccessType

Open Access Dissertation

Document Type

dissertation

Degree Name

Doctor of Philosophy (PhD)

Degree Program

Organismic and Evolutionary Biology

Year Degree Awarded

2020

Month Degree Awarded

May

First Advisor

Stephen D. McCormick

Subject Categories

Comparative and Evolutionary Physiology | Endocrinology | Integrative Biology | Zoology

Abstract

Lamprey represent the most basal living example of a vertebrate animal which regulates its internal fluid and ion homeostasis. This phylogenetic position among vertebrates makes lamprey an important model organism for understanding the basal state, and thus the evolution, of physiological systems such as the mechanisms of osmo- and ionoregulation and the endocrine factors controlling them. Sea lamprey (Petromyzon marinus) are an anadromous fish, migrating from freshwater (FW) to seawater (SW) as juveniles, then returning back upstream as mature adults to spawn. Surviving this transition from a solute-poor FW environment to a solute-concentrated SW environment requires many changes to osmo- and ionoregulatory mechanisms, which are driven, in part, by signaling from corticosteroid hormones. Much of this dissertation examines the molecular mechanisms for osmo- and ionoregulation in the lamprey gill and intestine and how corticosteroids control osmoregulatory processes in these tissues. Additionally, effect of temperature on osmoregulation, and the corticosteroid response to handling and thermal stressors are also examined. I report the results of experiments that were designed to identify molecular and organismal processes driving physiological acclimation to FW or SW residence. Special attention was given to understanding the endogenous nature of sea lamprey physiology, particularly regarding the development of the ability to survive and osmoregulate in SW that occurs during the larvae-to-juvenile metamorphosis. In Chapter 1, I offer an introduction to basic sea lamprey biology and physiology, including background on osmoregulation and corticosteroid action in fishes. In Chapter 2, I functionally characterize a critical ion transporter in the gills of SW-acclimated fishes responsible for Cl^- secretion, the Na⁺/K⁺/2Cl^- cotransporter (NKCC1). I demonstrate that (i) a membrane-bound NKCC1 is upregulated in the gills of sea lamprey during metamorphosis in preparation for SW migration; (ii) the timing of gill NKCC1 upregulation corresponds to the upregulation of another critical ion transporter and biomarker of ionoregulatory activity in fish gills, Na⁺/K⁺-ATPase (NKA), as well as the acquisition of SW tolerance; and (iii) pharmacological inhibition of NKCC1 markedly decreases SW tolerance in juvenile sea lamprey. In Chapter 3, I describe branchiometric changes that occur during the sea lamprey metamorphosis and SW acclimation, such as an increase in the branchiosomatic index (percentage of total body weight contributed by the gills) and a redistribution of the gill pouch-specific contribution to total gill NKA activity. In Chapters 4 and 5, I characterize 11-deoxycortisol as the endogenous corticosteroid hormone that controls osmo- and ionoregulation in the gills and intestine of sea lamprey. I show that (i) 11-deoxycortisol and its corticosteroid receptor (CR) are upregulated during metamorphosis and after exposure to SW; (ii) that the CR present in the gill and intestine are highly specific to binding by 11-deoxycortisol; and (iii) only 11-deoxycortisol (and not deoxycorticosterone, the other endogenous corticosteroid in lamprey blood) can upregulate osmo- and ionoregulatory mechanisms and SW tolerance in metamorphosing sea lamprey. In Chapter 6, I describe the glucose stimulating action of 11-deoxycortisol. I demonstrate that (i) lamprey responding to acute stress upregulate circulating 11-deoxycortisol and glucose in the blood plasma; (ii) only treatment with 11-deoxycortisol (and not deoxycorticosterone) increases plasma glucose; and (iii) among other tissues, the kidney uniquely expresses the transcriptional markers of steroidogenesis. Finally, in Chapter 7, I investigate the osmoregulatory capacity of post-metamorphic juvenile sea lamprey throughout springtime water warming and assess thermal tolerance of juvenile sea lamprey. I report that (i) elevated levels of gill NKA activity and SW tolerance persist well into the spring; (ii) survival after SW entry in late-spring is affected by temperature; and (iii) that juvenile sea lamprey can tolerate temperatures above 30 °C but begin showing signs of thermal stress, such as upregulation of heat shock proteins, at temperatures below their critical thermal maximum. Taken together, this dissertation contributes a substantial body of work regarding mechanisms of epithelial ion transport and corticosteroid action in the most basal vertebrate group. This dissertation describes that a single endogenous corticosteroid, 11-deoxycortisol, has a critical role in promoting the development of osmo- and ionoregulatory mechanisms during metamorphosis that confer survival in SW. This work will be of interest to scientists from a range of disciplines including physiology, endocrinology, evolutionary biology, developmental biology, and ecology, as well as conservationists and managers working with sea lamprey.

DOI

https://doi.org/10.7275/17602749

Recommended Citation

Shaughnessy, Ciaran A. S., "PHYSIOLOGY OF A BASAL VERTEBRATE, THE SEA LAMPREY (PETROMYZON MARINUS): OSMOREGULATION AND CORTICOSTEROID ACTION" (2020). Doctoral Dissertations. 1953.
https://doi.org/10.7275/17602749 https://scholarworks.umass.edu/dissertations_2/1953

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