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The Society for Integrative and Comparative Biology
Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales1
1 Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, California 93106-9610
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The goal of my research program is to employ biochemical and molecular techniques to gain ecological insight into the role of temperature in setting species' distribution patterns in the marine environment. Our central focus is the study of the environmental regulation of gene expression, where we are particularly interested in a set of inducible molecular chaperones, the heat-shock proteins (Hsps), and how the expression of these genes varies with the thermal history of organisms in natural populations. The primary study organisms are intertidal invertebrates and marine fish that experience dramatic changes in body temperature on varying temporal and spatial scales. In this review, I present studies that address the variable expression of Hsps, how these genes are differentially regulated in ectothermic animals in response to ecologically relevant temperature conditions, and how such plasticity in gene expression contributes to physiological plasticity in the environment.
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INTRODUCTION |
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For ectothermic marine animals, environmental temperature has a pervasive impact and influences function at all levels of biological organization, from the organismal to the molecular (Hochachka and Somero, 2002
). Environmental temperature also impacts larger scale processes such as biogeographical distribution patterns (Brown, 1984; Brown et al., 1996; Gaston, 2003) and species interactions (Sanford, 1999). The proximate physiological mechanisms and interacting forces that are drivers for these large-scale patterns are largely unknown. However, since environmental temperature is such an obvious candidate, ecological physiologists have made progress by targeting temperature-sensitive physiological processes and, consequently, thermal biology has been at the center of research examining large scale patterns of physiology in natural populations of marine organisms (e.g., Helmuth et al., 2002; Sokolova and Pörtner, 2003; Sorte and Hofmann, 2004). In general, these studies have originated out of an interest to understand how species range boundaries are determined and, from a more applied ecological perspective, how species distribution patterns might be altered by climate change (Fields et al., 1993; Barry et al., 1995; Southward et al., 1995; Sagarin et al., 1999; McCarty, 2001; Pörtner et al., 2001; Helmuth et al., 2002; Thompson et al., 2002; Kennedy et al., 2002; Hawkins et al., 2003; Parmesan and Yohe, 2003; Root et al., 2003; Stillman, 2003).
The application of ecological physiology practices at large spatial scales—sometimes termed macrophysiology (Chown et al., 2004)—is an active area of research in marine ecosystems. As a result of this work, two central questions are emerging: (1) how do physiological traits vary over large spatial scales, and (2) what is the ecological significance of the observed variation? In this review, I address how work in my research program has touched upon these two questions using biochemical and molecular approaches to understand the response to temperature at varying spatial scales. The examples described here use organisms from coastal marine ecosystems. The mechanistic focus, i.e., the temperature sensitive physiological process under study, is the heat-shock response (HSR), a molecular-level gene activation event that occurs in cells in response to elevated and abnormally high temperatures (Lindquist, 1986). Our studies have addressed the patterns of heat-shock protein (Hsp) gene expression in natural populations of marine invertebrates and fishes, and have examined the ecological implications for the observed patterns. The ultimate goal of these studies is to use a molecular physiology approach to examine organismal response to the thermal environment and to use these data to gain insight into how Hsps contribute to setting species distribution patterns in the marine ecosystem, ranging from microhabitat scale to large-scale biogeographical patterns.
In this review, three aspects of studies on Hsps are presented, each addressing an aspect of the regulation or role of Hsp gene expression in the environment at a different spatial or temporal scale. First, I address the plasticity of Hsp gene expression in ectothermic animals on microhabitat to local scales. Studies of mussels living in the rocky intertidal zone and of estuarine fishes have shown that the transactivation of Hsp gene expression is sensitive to the thermal history of the organism and changes on the microhabitat to local scale. Second, using a macrophysiology approach, I discuss how Hsps have been used to test whether coastal marine species are more stressed at the extremes of their biogeographical range. Finally, I discuss how, in the most extreme case across a distinct phylogeographic boundary, the Antarctic Polar Front, the expression of Hsps has been lost in notothenioid Antarctic fishes as compared to closely-related notothenioid species from the cool-temperate coastal waters of New Zealand.
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OVERVIEW |
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Studies of the HSR have been used to examine the response of organisms to environmental temperature at numerous ecological scales (for reviews see Sanders, 1993
; Hofmann, 1999; Feder and Hofmann, 1999; Hofmann et al., 2002; Halpin et al., 2002; Dahlhoff, 2004). The primary focus of the research described in this review examines patterns of Hsp gene expression (a physiological trait) and then explores the ecological implications of these patterns (variations in distribution and influence on species' range boundaries). With regard to the spatial studies in marine coastal ecosystems, we are attempting to link physiological response to species' performance in order to infer a significant role of temperature in setting species biogeographic ranges (Fig. 1). The impetus to use Hsps as a study system was largely due to their cellular role in protein homeostasis (Wickner et al., 1999) and protein folding (Fink, 1999; Hartl and Hayer-Hartl, 2002), combined with the observation that the organismal response to temperature could translate into variable costs of living in a particular thermal habitat (Huey, 1991). In this context, the analysis of Hsps is a biochemical indicator for the degree of protein unfolding that a cell is experiencing, an indirect measure of protein damage. In contrast, measurement of a second biochemical indicator—ubiquitin (Ub) conjugates—is a direct measure of protein loss via the Ub/proteasome pathway (Ciechanover, 1998). Taken together, these two measures have created a picture of how thermal heterogeneity in coastal marine ecosystems can influence organismal physiology in a way that impacts organismal distribution. Research in my program has included investigations that explore the function of Hsps as molecular chaperones in ectothermic marine fish (Place and Hofmann, 2001; Zippay et al., 2004), that address the plasticity of Hsp induction temperatures via the temperature-sensitive nature of HSF1-mediated transactivation in ectotherms (Buckley et al., 2001; Buckley and Hofmann, 2002, 2004), and extrapolates to broader scale phenomena including how Hsps might play a role in setting species distribution patterns on a microhabitat to latitudinal scale (Helmuth and Hofmann, 2001; Sorte and Hofmann, 2004).
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Microhabitat to mesoscale: Studies of gradients of stress in the rocky intertidal zone
Intertidal mussels have proven to be an ideal study organism to address the expression of Hsps along environmental gradients on the microhabitat scale. Because the rocky intertidal is characterized by steep gradients of abiotic stress (Menge and Branch, 2001
), studies of mussels have allowed the examination of Hsp expression as it varies as a function of thermal heterogeneity on small scales. As sessile residents of the rocky intertidal zone, mussels have body temperatures that are known to vary widely as a function of seasonal and tidal cycles (Hofmann and Somero, 1995; Helmuth, 1998, 1999; Fitzhenry et al., 2004) and on various spatial scales (Halpin et al., 2002). This physiological and ecological profile has allowed us to monitor body temperature and Hsp gene expression in an attempt to determine what aspect of temperature is physiologically significant with regard to activating the Hsp genes. These studies have shown that Hsp expression displays plasticity and that the induction temperature changes with thermal history of the individual (Buckley et al., 2001). For example, recent field experiments on summer-acclimatized mussels (Mytilus californianus) have shown that hsp70 was induced in gill tissue only when body temperature reached a threshold value (somewhere above 23°C). In these experiments, mussel gill was sampled during a recovery phase—an 18 hr period when mussels were submerged in seawater following aerial exposure during low tide. In these mussels, hsp70 mRNA was only detected in mussel gill collected from the mussels when the maximal body temperature exceeded 23°C during the previous aerial exposure during low tide (Fig. 2). In addition, it is clear from Northern analysis that hsp70 transcript remained in the cells for longer than might be anticipated given the turnover of Hsp transcript that has been measured in other systems (e.g., DiDomenico et al., 1982). Hsp70 mRNA levels remained elevated in gill cells for hours longer than would be calculated given a 30-minute half-life that is often observed for Hsp transcript in other cell types; whether this long-lived pool of transcript is related to longer actual mRNA half-lives, or to continuous transactivation of the hsp70 genes is under study. Regardless of the exact mechanism, the functionally extended presence of mRNA in mussel gill may meet the increased chaperoning needs that these animals experience in response to daily bouts of extreme thermal stress during low tide.
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Presumably, the increased chaperone need is induced by exaggerated gill protein denaturation in response to elevated body temperatures during emersion. This observation has been confirmed using assays that assess the degree of protein that is degraded via the Ub-proteasome pathway (Wickner et al., 1999
; Ciechanover, 1998). Analysis of ubiquitinated proteins— proteins that are tagged with Ub and thus marked for degradation by the proteasome—has shown that there is a dramatic pulse of Ub-conjugated proteins during recovery from low tide (Fig. 3; Hofmann and Somero, 1996b). These recurring bouts of protein damage may have a significant impact on organismal energetics given the cost of protein homeostasis (Carter and Houlihan, 2001). Reciprocal transplant experiments in the rocky intertidal have shown that M. californianus grew more slowly at high intertidal sites as compared to low sites; the slow growth rates also correlated with higher levels of Ub conjugates in gill tissue, suggesting that the physiological stress experienced at the upper limits of the mussel bed impacted growth performance (G. Hofmann and B. Menge, unpublished data). However, it should be noted that these different site-specific growth rates may also be related to increased time to filter-feed for the mussels situated in the low zone.
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Overall, the studies on intertidal mussels have highlighted the plastic nature of the heat shock response and how it might differ markedly in eurythermal ectotherms as compared to model systems. Several past studies have shown that threshold induction temperature for Hsp synthesis, as determined by synthesis of the protein gene product, was not fixed for a given species, but varied with acclimation or acclimatization (e.g., Dietz, 1994
; Hofmann and Somero, 1996a; Buckley et al., 2001; Tomanek and Somero, 2002; Buckley and Hofmann, 2002). Currently, the precise mechanism that accounts for such plasticity has not been completely identified, but is most likely related to the activity of the transcription of the hsp genes. Further investigation of this process required that all the steps in hsp gene expression be examined—mRNA synthesis and the transactivation of the hsp genes. In addition, these steps needed to be studied in a eurythermal ectotherm that would be good subjects for controlled temperature acclimation experiments in the laboratory. Since M. californianus is not an ideal lab animal, we turned to a eurythermal fish, the highly eurythermal estuarine goby Gillichthys mirabilis, to study the activity of the transcriptional factor, heat-shock factor 1 (HSF1), as a function of varying thermal history (Buckley and Hofmann, 2002, 2004).
Plasticity of the HSR and studies of HSF1 in a eurythermal fish
Initial research on the regulation of the heat-shock response in G. mirabilis revealed a great deal of plasticity in the kinetics of the response (Dietz, 1994). The mechanism accounting for the plasticity has been linked to the temperature-sensitive activity of HSF1 (Buckley and Hofmann, 2002, 2004). A much studied transcriptional factor in model systems, HSF1 is a latent cytoplasmic transcription factor that becomes activated through trimerization in response to stress (Wu, 1995; Morimoto, 1998; Pirkkala et al., 2001; Nollen and Morimoto, 2002); in response to stress, HSF1 binds specifically to the heat-shock element (HSE), an inverted heptad repeat (5'-nGAAn-3') in the promoters of inducible hsp genes (Pelham, 1982; Xiao and Lis, 1988) and transactivates the Hsp genes. In the goby studies, we developed an electromobility shift assay (EMSA) to detect the DNA-binding of HSF1 during in vitro assays (Buckley and Hofmann, 2002). Preliminary studies on G. mirabilis HSF1 revealed that the intensity of binding, i.e., the number of HSF1 molecules in the population with in vitro DNA binding capability, was temperature sensitive in our assay system (Fig. 4). Further experimentation demonstrated that this sensitivity was translated into a thermal history-dependent plasticity where HSF1 activity correlated with the acclimation temperature of the fish (Fig. 5; Buckley and Hofmann, 2002). Here, after a 5-week acclimation period (at 13, 21 or 28°C) the temperature of HSF1 activation was positively correlated with acclimation temperature (Fig. 5). As shown qualitatively in Fig. 5, HSF1 activation peaked at 17–21°C in the 13°C acclimation group, at 21°C in the 21°C group, and at 33°C in the fish acclimated to 28°C. In addition, the levels of HSF1-HSE complexes in liver from the 13 and 21°C groups exhibited a decline at higher temperatures as compared to the 28°C group where the amount of HSF1 with DNA-binding activity remained elevated (see Buckley and Hofmann, 2002).
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From an organismal perspective, the goby HSF1 studies highlighted a constantly adjustable regulatory mechanism that was capable of altering Hsp gene expression to match existing thermal conditions. The regulatory loop or "thermostat" is thus capable of responding to the prevailing chaperone needs, dictated by the levels of thermally denatured and unstable proteins, in the cells of eurytherms via thermal sensitivity of the controlling transcriptional factor, HSF1. These results make particular sense in the light of studies that have shown that "too much of a good thing" in this case, over-expression of Hsps, can be deleterious to cell function (Feder et al., 1992
). Thus, the ability to control Hsp synthesis that is commensurate with protein degradation rates is a process that matches chaperone pools with chaperoning requirements in eurythermic cells.
Macrophysiology and Hsps: latitudinal studies of the marine dogwhelk Nucella canaliculata
Just as macroecology explores patterns of distribution and abundance on large spatial scales (Brown, 1995), macrophysiology is also a pursuit of some ecological physiologists—those trying to explain functional variation or changes in performance at large spatial scales in the environment (Chown et al., 2004). The inference here is that the physiological trait has a selective value, and thus contributes to success across the species range and over environmental gradients encountered by a particular species. For example, in marine systems, physiologists have asked how processes of adaptation or acclimation underpin species distribution patterns that are observed in the rocky intertidal zone (reviewed in Somero, 2002) and what role animal thermotolerance might play on the biogeographic scale (reviewed in Pörtner, 2002). In addition, although large-scale patterns of distribution and physiological traits have been addressed for decades (e.g., Barnes, 1958; Newell, 1970), renewed interest in large-scale patterns of physiological traits is linked to interest in predicting the response of species to climate change. If we are to understand how species' range boundaries may shift in response to environmental change, we must first understand the physiological traits that explain the existing biogeographic patterns.
Studies of Hsps, genes with temperature-sensitive transactivation patterns, have the potential to contribute to macrophysiological studies in the marine environment because they can indicate at what temperature a particular species becomes thermally stressed. For example, in a study on the marine dogwhelk Nucella canaliculata, Sorte and Hofmann (2004) compared the physiological status of individuals in the center of the range of this invertebrate (sites on the central Oregon coast) vs. individuals from the southern boundary of the species (sites on the central California coast) by contrasting levels of Hsp70 in foot tissue. In these studies, physiological stress levels, as indicated by immunochemically determined levels of Hsp70 protein, were inversely related to snail abundances (Sorte and Hofmann, 2004). Levels of Hsp70 were higher in N. canaliculata collected at the range-edge sites as compared to those from the range-center sites (Fig. 6). Since past studies had suggested that emersion times would vary for intertidal organisms as a function of latitude (Helmuth et al., 2002), we attempted to minimize the effects of regional differences in tidal regime by our choice of field sampling dates. Nucella collections were performed at the range-edge sites in mid-April and at the range-center sites in mid-May. At the time of collection, both regions were in the middle of periods of minus tides, and low tides occurred early in the morning at all sites (see Sorte and Hofmann, 2004 for details). Inevitably, there were regional differences in conditions (e.g., weather, wave splash), but this collection strategy was the best approach to controlling for latitude-dependent exposure time.
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The mapping of physiological traits onto species' biogeograpical range is a rewarding, but challenging, area of research. There is a great deal of complexity inherent in this pursuit and interpretation of data and the development of appropriate sampling protocols is a challenge. However, there are already excellent examples of research that have documented features such as growth and population dynamics on biogeograpical scales—for example, at southern range limits (e.g., Barnes, 1958
; Henderson and Seaby, 1999; Westerbom et al., 2002; Sorte and Hofmann, 2004), and where northern range limits have expanded (Zacherl et al., 2003). A significant challenge in the future will be to expand and diversify the physiological traits that are examined and thereby increase the resolution and diversity of these surveys. One effective strategy may be to combine the use of multiple assays to assess organismal health (e.g., Downs et al., 2000, in corals). Another fruitful strategy would involve genomics approaches where physiological signatures of response to a variety of abiotic factors can be determined simultaneously (e.g., Gracey et al. 2001; Feder and Mitchell-Olds 2003; see Gracey and Cossins, 2003 for a review). Further, these genomic-scale patterns can then be correlated to more organismal-level indicators of performance such as growth or nutritional status. Another significant challenge in macrophysiological studies in marine ecosystems arises in the form of geographic or oceanographic complexity as these relate to barriers to distribution in the marine environment. For example, Gaylord and Gaines (2000) have shown that current patterns, as opposed to seawater temperature, may have a dominant role in creating species distribution patterns that are found around Point Conception, a well known biogeographic barrier on the Pacific coast. Finally, physiological studies will need to integrate with population structure in order to examine the role of local adaptation on these large spatial scales (e.g., Sanford et al., 2003). Still, despite all the hurdles in this area of research, macrophysiological approaches have a great deal to contribute to our understanding of marine ecosystems and how the physiological tolerances of the resident species will allow them to respond to temperature change in the future.
Biogeographic scale: Antarctic fish vs. New Zealand fish
Members of the suborder Notothenioidei also provide an opportunity to observe how physiological traits and performance change over an environmental temperature gradient, in this case, a large oceanographic boundary, the Antarctic Polar Front (Eastman, 1993). In this case, the macrophysiology studies are performed on closely related species of notothenioid fishes from the coastal waters of the Southern Ocean and New Zealand that are differentially adapted to temperature (Hofmann et al., 2004). The Antarctic species live in subzero seawater with a steady –1.86°C temperature; in contrast, the New Zealand species encounter temperatures from +8 to +15°C on an annual basis. Given the environmental temperatures of the fish and the observation that threshold induction tends to track adaptation temperature in ectotherms (Feder and Hofmann, 1999), one would predict that cells in the Antarctic species would express Hsp genes at temperatures just a few degrees above zero. Surprisingly, earlier studies found that a representative Antarctic notothenioid, Trematomus bernacchii, did not exhibit a classical heat shock response at all, in either whole body or isolated cell preparations (Hofmann et al., 2000). More recent investigations have found that this unusual occurrence (the HSR has been reported in every organism examined save a freshwater Hydra (Brennecke et al., 1998) and Antarctic notothenioids), may be explained by a recruitment of the stress-inducible genes into constitutive expression. Northern analysis has shown that tissues from T. bernacchii (Fig. 7; Place et al., 2004) and other species (data not shown; Place and Hofmann, 2005) possess hsp70 mRNA even after immediate capture from the under the sea ice. Similarly sampled New Zealand fishes did not exhibit this trait (Fig. 7), and only contain hsp70 mRNA when cells or tissues have been heat stressed (Fig. 8; Hofmann et al., 2004). Currently, the regulatory mechanism for the alteration in transactivation of the stress-inducible member of the 70 kDa-Hsp gene family is unknown. Studies on HSF1 in isolated hepatocytes have shown that HSF1 is present and displayed DNA-binding activity at control temperatures (Buckley et al., 2004), suggesting that the hsp70 gene has been recruited into constitutive expression (Place et al., 2004). Taken together, these results indicate that the Antarctic cells appear to have a normal contingent of transcriptional apparatus that is functioning in an unexpected fashion. A potential explanation lies in the key signal for Hsp induction—the presence of denatured or nonnative proteins in cells (Ananthan et al., 1986). Preliminary experiments have shown that gill and liver tissue of T. bernacchii contained unexpectedly high levels of Ub conjugates and it may be that high levels of unstable proteins has resulted in permanent up-regulation of these otherwise exclusively stress-inducible genes (Place et al., 2004). Although this observation may seem unusual, other eukaryotic cells have been shown to up-regulate the expression of molecular chaperones in response to extreme cold (Kandror et al., 2004). Ironically, these results suggest that extremely cold habitats, and the resulting cold denaturation of proteins, may be as challenging to protein homeostasis as protein perturbing thermal stress in temperate habitats.
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SUMMARY |
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The study of Hsps, their regulation and expression in natural populations has resulted in increased insight into the thermal biology of marine invertebrates and fish. These studies have highlighted the complexity of the link between the ecology and physiology of eurythermal ectotherms, illustrating that past thermal history has a significant impact on the patterns of expression of the Hsp genes. Research in this area has contributed to our understanding of the physiologically significant aspect of the "thermal signal" of environmental temperature for a variety of marine ectothermic animals. Finally, the variation in this physiological trait—the up-regulation of Hsp genes—has served as a measure of relative physiological condition in large-scale, macrophysiological studies in marine invertebrates. Coupled with additional techniques that describe more physiological processes, eco-physiological approaches stand to make significant contributions to understanding the mechanisms, temperature-related or not, that set large-scale biogeographic distribution patterns of organisms in nature.
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ACKNOWLEDGMENTS |
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I thank members of my lab group—Dr. Brad Buckley, Dr. Susan Lund, Dr. Sean Place, Cascade J. B. Sorte, and Mackenzie L. Zippay—who contributed to the research presented here. In addition, I am indebted to Drs. Art DeVries, Martin Feder, Steve Gaines, Patricia Halpin, Brian Helmuth, Bruce Menge, Dov Sax, David F. Smith, George Somero and Ali Whitmer for discussions, ideas, and important collaborations during the course of this work. These studies were supported by National Science Foundation grants OCE 9696022, IBN 0096100, OPP 0301927, and support from Susan and Bruce Worster to GEH as the Worster Scholar at UC, Santa Barbara.
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FOOTNOTES |
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1 From the Symposium Integrative Biology: A Symposium Honoring George A. Bartholomew presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 5–9 January 2004, at New Orleans, Louisiana
2 E-mail: hofmann{at}lifesci.ucsb.edu
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