Acyl composition of muscle membranes varies with body size in birds
1 Metabolic Research Centre, University of Wollongong, Wollongong, NSW 2522,
Australia
2 Department of Biological Science, University of Wollongong, Wollongong,
NSW 2522, Australia
3 Department of Biomedical Science, University of Wollongong, Wollongong,
NSW 2522, Australia
* Author for correspondence (e-mail: hulbert{at}uow.edu.au)
Accepted 20 August 2002
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Summary |
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Key words: muscle phospholipid, polyunsaturate, docosahexaenoic acid, allometry, basal metabolism, maximum lifespan, bird
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Introduction |
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Intrigued by Gudbjarnason's observation, coupled with the knowledge that
the high metabolic rate of endothermic rats, compared to the low metabolic
rate of ectothermic lizards, was also associated with a high 22:6 content of
both liver and kidney phospholipids
(Hulbert and Else, 1989) as
well as liver mitochondrial phospholipids
(Brand et al., 1991
), Couture
and Hulbert (1995a
)
investigated whether Gudbjarnason's observation might be part of a more
general body-size-related phenomenon. They measured the acyl composition of
tissue phospholipids from five species of mammal of different sizes, ranging
from mice to cattle. They confirmed Gudbjarnason's original observation and
found it was indeed part of a more general relationship and not restricted to
the heart. Tissue phospholipids from the small mammals were more
polyunsaturated than those from the large mammal species whilst the
phospholipids from large mammals were more mono-unsaturated than those from
small mammals. This relationship was present in all tissues examined (heart,
liver, kidney and skeletal muscle) except the brain. Brain phospholipids were
highly polyunsaturated in all the mammal species examined, irrespective of the
species body size.
More recently a collation and review of published data for mammals
(Hulbert et al., 2002) has
shown that, excluding the brain, the tissue phospholipids of different sized
mammals show no allometric trend in their total percentage of unsaturated acyl
chains, but statistically significant allometric declines in their degree of
unsaturation (i.e. in their unsaturation index; the total number of double
bonds per 100 acyl chains) with increasing body size. This is predominantly
due to very significant and substantial allometric decreases in the content of
the highly polyunsaturated n-3 acyl chain, docosahexaenoic acid (22:6
n-3). The allometric exponents for the 22:6 relationships varied from
-0.19 for liver phospholipids to -0.40 for skeletal muscle phospholipids.
These probably represent the largest body-size-related variation of body
composition recorded for mammals and the allometric exponents obtained are
similar to those for mass-specific metabolic rate of mammals (Kleiber,
1961).
Over the last decade it has become obvious that much of the energetic cost
of life is associated with the maintenance, by various membrane-associated
transport systems, of thermodynamically unfavourable transmembrane ion
gradients. Two important examples are the plasmalemmal Na+ gradient
and the mitochondrial H+ gradient (e.g.
Clausen et al., 1991;
Brand et al., 1994
;
Rolfe and Brown, 1997
).
Recently, it has been suggested that the acyl composition of membranes has an
important influence on the molecular activity of many membrane proteins,
including membrane transport systems, and that in this way membrane lipids may
act as pacemakers for metabolism of different species
(Hulbert and Else, 1999
). The
functional significance of the finding of more polyunsaturated membranes in
small mammals and its potential role in the allometric variation in metabolic
rate of mammals have recently been discussed
(Hulbert and Else, 2000
), and
the effects of membrane lipids on the molecular activity of membrane proteins,
such as the Na+,K+-ATPase, may be related to their
effects on the physical aspects of molecular packing in membranes
(Wu et al., 2001
).
If the degree of membrane polyunsaturation is indeed a pacemaker for
metabolic rate, then similar allometric variation in membrane acyl composition
should exist in other groups of animals that also show body-size-related
variation in their metabolism. One such group are the birds. Relatively little
is known of the acyl composition of tissue phospholipids from birds. Here we
report the findings of a study of the acyl composition of phospholipids from
the skeletal muscle of eight species of bird ranging in mass from the 13 g
zebra finch to the 34 kg emu. The results for these eight species have been
combined with those recently published for a 3 g hummingbird
(Infante et al., 2001) and
allometric relationships determined. These species represent an approximately
11000-fold difference in body mass between the smallest and largest birds.
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Materials and methods |
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Total lipids were extracted from the muscle samples by standard methods
(Folch et al., 1957) using
ultrapure-grade chloroform and methanol (2:1, v/v) containing butylated
hydroxytoluene (0.01% w/v) as an antioxidant. For each preparation
phospholipids were separated from neutral lipids using Sep-pak silica
cartridges (Waters, Milford, MA, USA). The acyl composition of each
phospholipid fraction was determined by methods described in detail elsewhere
(Pan and Storlien, 1993
).
The results obtained were combined with those for breast muscle
phospholipids from the ruby-throated hummingbird Archilochus colubris
taken from Table 2 of Infante et al.
(2001). In this table there
are some misprints; the correct values for 20:2 n-6, 20:3
n-6 and 20:4 n-6 are, respectively, 0%, 0.11% and 5.87% (J.
T. Brenna, personal communication). Body mass and BMR values for this
hummingbird species were taken from Lasiewski
(1963
). The mass-specific BMR
values for the other species were either calculated from published allometric
equations (Lasiewski and Dawson,
1967
), obtained from the literature or from as-yet-unpublished
studies. All figures and allometric equations were produced using KaleidaGraph
(version 3.0.5) software (Abelbeck Software). The statistical significance of
each relationship was determined from the correlation coefficient given with
each allometric equation. All experiments were approved by the University of
Wollongong Animal Experimentation Ethics Committee.
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Results |
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When the acyl composition of skeletal muscle phospholipids from these nine species were compared the phospholipids from the smaller species were significantly more unsaturated (as represented by the unsaturation index, Fig. 2A); however, there was no significant body-size-related variation in the total percentage of unsaturated acyl chains (Fig. 2B). On average, the skeletal muscle phospholipids of birds possess 62% unsaturated acyl chains. There was a significant allometric increase in the mono-unsaturate content in the larger species, whilst the total polyunsaturate content was relatively constant irrespective of species body mass (Fig. 2C). Whilst there was a non-significant trend for n-6 polyunsaturated fatty acid (PUFA) content to increase, n-3 PUFA content of skeletal muscle phospholipids showed a significant decrease with increasing body mass (Fig. 2D). From the allometric slopes of the statistically significant relationships in Fig. 2 we can calculate that for every doubling of bird body mass, there is on average a 2.7% decrease in the number of double bonds per 100 acyl chains, a 5.0% increase in the mono-unsaturate content and a 8.0% decrease in n-3 PUFA content of skeletal phospholipids.
|
In Fig. 3 are plotted the
allometric relationships for some of the major individual acyl chains. For the
saturated acyl chains (Fig. 3A)
there was no significant trend in stearic acid (18:0) content but there was a
significant allometric decline in palmitic acid (16:0). For the two 18C
mono-unsaturates (Fig. 3B) there were opposing trends but only the relationship for the more common
n-9 oleic acid was statistically significant. Both of these
mono-unsaturates can be synthesised from the saturated palmitic acid (16:0) by
the sequential action of the elongase and the 9-desaturase enzyme
systems. Whether vaccenic acid (18:1 n-7) or oleic acid (18:1
n-9) is formed will depend on the sequence that these two enzyme
systems act on 16:0. When 16:0 is elongated before being
9-desaturated,
18:1 n-9 is the product, whereas when
9-desaturation occurs
before elongation then 18:1 n-7 is the resultant product. The
significant allometric increase in 18:1 n-9 may indicate a greater
elongase activity in the larger bird species. Although it was not
statistically significant there was a tendency for the ratio of 18:0/16:0
(which is sometimes used as an indicator of elongase activity) to be greater
with increasing body mass (results not shown).
|
The allometric relationships describing the relative content of the two
main n-6 PUFAs are shown in Fig.
3C. The relationship for linoleic acid (18:2 n-6) was not
statistically significant and the apparent slope of this relationship is
solely due to the very low 18:2 n-6 content reported for the
hummingbird by Infante et al.
(2001). This value seems
anomalous compared to those for the other species. There is a significant
positive allometric relationship for arachidonic (20:4 n-6) content
of skeletal muscle in birds. In most species the 20:4 n-6 content was
substantially less than the content of its precursor 18:2 n-6. This
was not the case for the n-3 PUFAs, where in all species the content
of the highly polyunsaturated docosahexaenoic acid (22:6 n-3) was
greater than the content of its precursor n-3 PUFAs. In
Fig. 3D are plotted the
allometric relationships for two n-3 polyunsaturates. Eicosapentanoic
acid (20:5 n-3) content did not vary with body mass but
docosahexaenoic acid (22:6 n-3) showed a very significant negative
allometric relationship with an exponent of -0.28. Such an exponent means that
for every doubling of body mass in birds there is a 17.6% decrease in the
content of 22:6 n-3 in skeletal muscle phospholipids. This
relationship represented the steepest allometric relationship of any acyl
chain examined. Because of its highly desaturated nature, when present in
substantial amounts this acyl chain is a major contributor to the overall
unsaturation index of skeletal muscle phospholipids. In
Fig. 4 is plotted the
calculated percentage contribution of 22:6 n-3 to the unsaturation
index for each species and this is inversely related to body mass, varying
from approximately 70% in the hummingbird to less than 6% in the emu.
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Discussion |
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The results of this study further collaborate the observation that, in
vertebrates, metabolically active systems have polyunsaturated membranes,
whilst in metabolically inactive systems, membranes are less polyunsaturated
but more monounsaturated (Hulbert and
Else, 1999). This can be observed in
Fig. 5, where there is a
significant negative correlation between the mono-unsaturate content of
skeletal muscle phospholipids of the bird species and their mass-specific BMR
and significant positive correlations of the unsaturation index, n-3
polyunsaturate content and 22:6 content of skeletal muscle phospholipids and
BMR. In view of the strong input from 22:6 into unsaturation index, the three
positive correlations are all describing the same phenomenon.
|
In the present study we have extrapolated our finding in pectoral muscle to
skeletal muscle in general. Nothing is known about the phospholipid acyl
composition of different muscles in birds. In the rat there are only small
differences in the acyl composition and no significant difference in the
unsaturation index and docosahexaenoic acid content of phospholipids from
soleus or EDL muscle, although these muscles differ substantially in their
fibre type composition (Ayre and Hulbert,
1996; Blackard et al.,
1997
).
Whether other tissues of birds show the same body-size-related variation in phospholipid acyl composition that is observed in skeletal muscle, as in mammals, is not yet known. Similarly, the degree of allometric variation in the acyl composition of subcellular membranes of tissues from birds has not yet been studied systematically and is thus not known, although liver mitochondrial membranes from birds show an allometric decline in their degree of unsaturation with body size (M. D. Brand, P. L. Else and A. J. Hulbert, unpublished observations), similar to our observations for total phospholipids from skeletal muscle.
Higher animals lack the 12- and
15-desaturases found in
plants and thus both the n-6 and n-3 polyunsaturated acyl
chains must either be obtained from their diet or from their gut microbes
(which presumably are capable of de novo PUFA synthesis). Most
knowledge in this area comes from research on mammals, and whilst very little
is known for birds it is assumed that the same processes occur. Once in the
body the 18C chain versions of both of these types of polyunsaturates can
generally be both elongated and further desaturated by appropriate enzyme
systems, although this is not universally true for all animal species. The
relative occurrence of different acyl chains in membranes is a regulated
phenomenon, and although dietary deficiency of particular types of fatty acids
will have an influence, it is generally difficult to substantially change
membrane acyl composition by dietary manipulation. In some situations, there
seems to be simple competition between n-6 and n-3
polyunsaturates, and their relative abundance in muscle membranes is strongly
influenced by their relative presence in the diet (e.g.
Pan and Storlien, 1993
). Some
of the variation observed in the present study is probably related to the
generally small influence of diet on membrane acyl composition. None of the
birds would appear to have had a diet deficient in polyunsaturates, in that
mead acid (20:3 n-9) was absent in most samples and present in
negligible amounts (<0.1%) in the currawong and the goose. This unusual
acyl chain is only synthesised in significant amounts when normal n-6
and n-3 polyunsaturates are absent and its appearance is used as an
indicator of such dietary essential fatty acid (PUFA) deficiency. The fatty
acyl composition of the diet can influence the acyl composition of
phospholipids, but not to the same degree that it influences the composition
of triglycerides. However, differences in diet are unlikely to explain the
allometric variation in docosahexaenoic content of phospholipids observed in
the current study, as this long-chain n-3 polyunsaturate would not be
expected to be a significant component of the diet of any of the bird species
examined.
Whilst the synthesis and modification to many acyl chains appears to occur
in the endoplasmic reticulum, the synthesis of docosahexaenoic acid appears to
be more complex and is not currently agreed. It has been suggested that,
whilst 5 and
6-desaturases definitely exist, the
4-desaturase (which in some proposed schemes is necessary for synthesis
of 22:6 n-3) does not in fact exist, and that the synthesis of 22:6
n-3 involves a single cycle of ß-oxidation of 24:6 n-3
in peroxisomes (for a review, see
Sprecher, 2000
). The synthesis
of this important highly unsaturated acyl chain appears to be different and
more complex than that of most other acyl chains, and regulated
differently.
Membrane acyl composition is also regulated by constant membrane
remodelling. In rat liver cells only four molecular species of
phosphatidylcholine and phosphatidylethanolamine are synthesised de
novo; all other molecular species are produced by
deacylationreacylation processes
(Schmid et al., 1995). These
processes are very rapid, in that within minutes of being added to the culture
medium, labelled acyl chains appear in the plasma membrane phospholipids of
cultured cells (Chakravarthy et al., 1986). The roles of any of these enzyme
systems in determining the allometric variation in membrane acyl composition
is currently unknown for both mammals and birds.
The functional significance of this body-size-related variation in membrane
acyl composition is probably related to the long-known allometric variation in
metabolism. For example, the activity of the sodium pump varies allometrically
with body size in mammalian liver and kidney slices
(Couture and Hulbert, 1995b),
the molecular activity of the Na+,K+-ATPase from
endothermic vertebrates is several times that from ectothermic vertebrates
when measured at the same temperature
(Else et al., 1996
) and in
`species-crossover' experiments between rats and toads it has been
demonstrated that the membrane lipids are major determinants of this
difference in molecular activity (Else and
Wu, 1999
). Using preparations from two tissues that have a high
tissue density of sodium pumps, namely kidney and brain, it has recently been
shown that the higher polyunsaturate content of rat compared to toad membranes
may be influencing the high molecular activity in mammalian tissues
via effects on the molecular packing of membrane lipids
(Wu et al., 2001
). Similarly,
a number of studies have now suggested a connection between liver
mitochondrial membrane polyunsaturation and liver mitochondrial proton leak
between both endothermic and ectothermic vertebrates
(Brand et al., 1991
;
Brookes et al., 1998
) as well
as between mammals of different body size
(Porter et al., 1996
). Even
the difference in mitochondrial proton leak between the different tissues of
the rat appears to be related to differences in the degree of polyunsaturation
of mitochondrial membranes, with skeletal muscle having the greatest
unsaturation index, the highest docosahexaenoic acid content and the greatest
proton leak of all tissues examined (Rolfe
et al., 1994
). Another significant component of metabolism,
especially in muscle, is the cost of maintaining trans-membrane
Ca2+ gradients, and docosahexanoate-containing phospholipids have
been suggested to be important for very active Ca2+-ATPases
(Infante, 1987
;
Infante et al., 2001
).
Polyunsaturated acyl chains in membranes may be important determinants not
only of the pace of life but also for the length of life. Not only do they
probably result in a greater consumption of oxygen but they are also important
substrates for damage by the free radicals produced by this enhanced oxygen
consumption, resulting in lipid peroxides. Polyunsaturates are especially
susceptible to lipid peroxidation and their double bonds are located in the
very place that most reactive oxygen species are produced, namely deep in the
mitochondrial membrane bilayer. In mammals, the body-size-related variation in
acyl composition of heart phospholipids
(Pamplona et al., 1999c) and
liver mitochondrial phospholipids
(Pamplona et al., 1998
) have
been shown to be strongly correlated with maximum lifespan. The low level of
phospholipid unsaturation in larger mammalian species has been related to a
lower level of lipid peroxidation and lipoperoxidative damage to tissue
proteins in these larger mammals, and has been suggested as a mechanism
involved in their longer maximum lifespans
(Pamplona et al., 2000
).
Although birds and mammals show similar body-size-related relationships in
the acyl composition of skeletal muscle phospholipids, there are some
differences in composition between these two endothermic groups of
vertebrates. If we compare a medium-sized species of bird and mammal (say 250
g body mass), the skeletal muscle phospholipids of the bird will possess 95%
of the unsaturated acyl content of the mammal but have an unsaturation index
that is 82% of the value for the mammal. The bird skeletal muscle
phospholipids will have 50% more mono-unsaturated and 15% less polyunsaturated
acyl chains than the mammal. The bird will have 12% more n-6 PUFA and
26% less n-3 PUFA than the mammal, with the consequence that the
ratio of n-3/n-6 in the bird will be about half the value
calculated for the mammalian muscle phospholipids. The docosahexaenoic acid
content of the bird muscle membranes will, on average, be approximately
two-thirds of that in the mammal. Whether these differences have functional
consequences is not known, but it is tempting to speculate that the
n-3 and n-6 differences may be related to the longer
lifespan of birds compared to mammals
(Holmes and Austad, 1995). It
has been proposed that the low unsaturation of pigeon mitochondria compared to
rat mitochondria, for both liver and heart, protects against lipid
peroxidation in the pigeon and is related to the much longer lifespan in the
pigeon than the rat (Pamplona et al.,
1996
,
1999a
). A comparison of heart
phospholipid acyl composition of the canary and the parakeet with the mouse
yielded similar results (Pamplona et al.,
1999b
).
Whether the allometric relationships found for the phospholipid acyl
composition of skeletal muscle of birds (this study) and mammals
(Hulbert et al., 2002) also
exist in skeletal muscle of ectothermic vertebrates is unknown. The bird and
mammal studies both involved vertebrates that have approximately the same body
temperature within each group. Any comparison of ectotherms of differing body
size would need to take the body temperature of the species into account, as
modification of membrane acyl composition is known to be one of the main
mechanisms of temperature acclimation in ectotherms (e.g.
Hazel and Williams, 1990
;
Hazel, 1995
).
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Acknowledgments |
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References |
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