Despite extensive research into thermal relationships of
ectothermic animals, there remain large gaps in our
understanding of how temperature affects the ability of
ectotherms to cope with pathogens through both specific and
nonspecific immune responses. Temperature affects both
specific and nonspecific immunity, so these thermal effects are
apt to be of considerable importance to ectotherms that
encounter variations in environmental temperature (see Le
Morvan et al., 1998 for a review). Low temperatures,
consistent with normal seasonal fluctuations, correlate with
increased pathogenesis in teleost fish (Baudouy et al., 1980;
Bly and Clem, 1992; Le Morvan et al., 1998). Most infectious
diseases occur over wide ranges of body temperatures and the
outcome of the pathogenesis is likely to depend on the
differential effects of change in temperature on the efficacy of
the immune response and the growth rate of the pathogen. In
4539 The Journal of Experimental Biology 206, 4539-4551
© 2003 The Company of Biologists Ltd
doi:10.1242/jeb.00706
The ability to heal superficial wounds is an important
element in an organism’s repertoire of adaptive responses
to environmental stress. In fish, motile cells termed
keratocytes are thought to play important roles in the
wound-healing process. Keratocyte motility, like other
physiological rate processes, is likely to be dependent on
temperature and to show adaptive variation among
differently thermally adapted species. We have quantified
the effects of acute temperature change and thermal
acclimation on actin-based keratocyte movement in
primary cultures of keratocytes from four species of
teleost fish adapted to widely different thermal conditions:
two eurythermal species, the longjaw mudsucker
Gillichthys mirabilis (environmental temperature range of
approximately 10–37°C) and a desert pupfish, Cyprinodon
salinus (10–40°C), and two species from stable thermal
environments, an Antarctic notothenioid, Trematomus
bernacchii (–1.86°C), and a tropical clownfish, Amphiprion
percula (26–30°C). For all species, keratocyte speed
increased with increasing temperature. G. mirabilis and C.
salinus keratocytes reached maximal speeds at 25°C and
35°C, respectively, temperatures within the species’
normal thermal ranges. Keratocytes of the stenothermal
species continued to increase in speed as temperature
increased above the species’ normal temperature ranges.
The thermal limits of keratocyte motility appear to exceed
those of whole-organism thermal tolerance, notably in the
case of T. bernacchii. Keratocytes of T. bernacchii survived
supercooling to –6°C and retained motility at
temperatures as high as 20°C. Mean keratocyte speed was
conserved at physiological temperatures for the three
temperate and tropical species, which suggests that a
certain rate of motility is advantageous for wound healing.
However, there was no temperature compensation in
speed of movement for keratocytes of the Antarctic fish,
which have extremely slow rates of movement at
physiological temperatures. Keratocytes from all species
moved in a persistent, unidirectional manner at low
temperatures but at higher temperatures began to take
more circular or less-persistent paths. Thermal
acclimation affected the persistence and turning
magnitude of keratocytes, with warmer acclimations
generally yielding more persistent cells that followed
straighter paths. However, acclimation did not alter the
effect of experimental temperature on cellular speed.
These findings suggest that more than one temperature-
sensitive mechanism may govern cell motility: the rate-
limiting process(es) responsible for speed is distinct from
the mechanism(s) underlying directionality and
persistence. Keratocytes represent a useful study system
for evaluating the effects of temperature at the cellular
level and for studying adaptive variation in actin-based
cellular movement and capacity for wound healing.
Key words: Antarctic fish, cell motility, cytoskeleton, notothenioid,
keratocytes, temperature.
Summary
Introduction
Influences of thermal acclimation and acute temperature change on the motility
of epithelial wound-healing cells (keratocytes) of tropical, temperate and
Antarctic fish
Rachael A. Ream
1
, Julie A. Theriot
1
and George N. Somero
2,
*
1
Biochemistry Department, Beckman Center, Room 473A, Stanford University School of Medicine, Stanford,
CA 94305-5307, USA and
2
Hopkins Marine Station, Pacific Grove, CA 93950, USA
*Author for correspondence (e-mail: somero@stanford.edu)
Accepted 4 September 2003