Transformation of metabolism with age and lifestyle in Antarctic seals: a case study of systems biology approach to cross-species microarray experiment

Abstract

BackgroundThe metabolic transformation that changes Weddell seal pups born on land into aquatic animals is not only interesting for the study of general biology, but it also provides a model for the acquired and congenital muscle disorders which are associated with oxygen metabolism in skeletal muscle. However, the analysis of gene expression in seals is hampered by the lack of specific microarrays and the very limited annotation of known Weddell seal (Leptonychotes weddellii) genes.ResultsMuscle samples from newborn, juvenile, and adult Weddell seals were collected during an Antarctic expedition. Extracted RNA was hybridized on Affymetrix Human Expression chips. Preliminary studies showed a detectable signal from at least 7000 probe sets present in all samples and replicates. Relative expression levels for these genes was used for further analysis of the biological pathways implicated in the metabolism transformation which occurs in the transition from newborn, to juvenile, to adult seals. Cytoskeletal remodeling, WNT signaling, FAK signaling, hypoxia-induced HIF1 activation, and insulin regulation were identified as being among the most important biological pathways involved in transformation.ConclusionIn spite of certain losses in specificity and sensitivity, the cross-species application of gene expression microarrays is capable of solving challenging puzzles in biology. A Systems Biology approach based on gene interaction patterns can compensate adequately for the lack of species-specific genomics information.

Transcriptome analysis of northern elephant seal (Mirounga angustirostris) muscle tissue provides a novel molecular resource and physiological insights

“…Despite these improvements, sequence-based resources are still lacking for many non-model species such as marine mammals, hampering molecular understanding of unique adaptations and physiology. Only a handful of marine mammal genomes have been sequenced, annotation remains a challenge, and few transcriptomes are available [ 15 - 22 ].…”

Convergent evolution of marine mammals is associated with distinct substitutions in common genes

“…Four genes ( PRKCA , PLCB4 , ROCK1 , MAPK10 ) in the Wnt signaling pathway were also present in the candidate aquatic adaptation gene list ( P = 0.007, Fisher’s exact test) ( Supplementary Table S6 ). Altered expression of genes associated with the Wnt pathway has been implicated in metabolic and structural transformation of Weddel seal skeletal muscle from a strictly terrestrial lifestyle as a pup to an aquatic lifestyle adapted for deep dives as adult animals 35 .…”

Fatty Acid use in Diving Mammals: More than Merely Fuel

“…Indeed, recent evidence has shown that the amount and type of lipids act as important initial regulators of myoglobin in diving mammals (De Miranda Jr. et al, 2012) with some indication of secondary regulation by activity level and calcium signaling (Kanatous et al, 2008b, 2009; Ptitsyn et al, 2010). In comparative animal studies, an increase of n− 3 PUFAs or a high n− 3 to n− 6 ratio of fatty acids was shown to prompt increases in calcium transport and calcium absorption in PUFA-deficient rats (Kruger and Horrobin, 1997; Weiss et al, 2005).…”

“…These constraints demand that the Antarctic divers be more tightly regulated with respect to their oxygen utilization; they must complete a dive cycle and find a breathing hole before their oxygen stores are depleted. Previous research has illustrated how these and open water divers are uniquely adapted to their environment and how energy is conserved even at the molecular level (Burns, 1996 ; Burns et al, 1998 ; Kanatous et al, 1999 , 2001 , 2002 , 2008a , b ; Burns et al, 2005 , 2007 ; Clark et al, 2006 , 2007 ; Noren et al, 2008b ; Ptitsyn et al, 2010 ; Trumble et al, 2010 ; Ponganis et al, 2011 ; Williams et al, 2011 ). For example, studies of adult Weddell seals, harbor seals ( Phoca vitulina ) and Steller sea lions ( Euematopias jubatus ) have revealed that their muscle adaptations to maintain a lipid based aerobic metabolism under the hypoxic conditions associated with breath-hold diving include: (1) an increased aerobic capacity (or one that is matched to routine levels of exertion), (2) a reliance on fatty acid catabolism for aerobic ATP production, (3) enhanced oxygen storage and diffusion capacity, and (4) a reduced dependency on blood-borne oxygen and metabolites (e.g., decreased capillary density) compared to terrestrial mammals (Davis et al, 1991 ; Davis and Kanatous, 1999 ; Kanatous et al, 1999 , 2001 , 2002 ).…”

“…In terms of skeletal muscle development, the cessation of weaning and commencement of diving in Weddell seals induces developmental changes in muscle physiology that parallel changes in activity. Preliminary microarray results indicate differential expression of RNA transcripts associated with various ontogenic signaling pathways, in addition to differences in transcripts associated with lipid metabolism, among age classes (Kanatous et al, 2008b ; Ptitsyn et al, 2010 ). These previous findings mirrored results describing significant changes in the lipid composition and potential utilization of fatty acids in skeletal muscle during these developmental stages (Trumble et al, 2010 ).…”