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Evolution of Mammalian Diving Capacity Traced by Myoglobin Net

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Evolution of Mammalian Diving Capacity Traced by Myoglobin Net RESEARCH ARTICLE SUMMARY READ THE FULL ARTICLE ONLINE Evolution of Mammalian Diving http://dx.doi.org/10.1126/ science.1234192 Capacity Traced by Myoglobin Cite this article as S. Mirceta et al., Science 340, Net Surface Charge 1234192 (2013). DOI: 10.1126/science.1234192 Scott Mirceta, Anthony V. Signore, Jennifer M. Burns, Andrew R. Cossins, Kevin L. Campbell, Michael Berenbrink* FIGURES IN THE FULL ARTICLE Fig. 1. Myoglobin net surface charge and Introduction: Evolution of extended breath-hold endurance enables the exploitation of the aquatic maximal muscle concentration in terrestrial, niche by numerous mammalian lineages and is accomplished by elevated body oxygen stores and semiaquatic, and aquatic mammals. morphological and physiological adaptations that promote their economical use. High muscle Fig. 2. Relationship between electrophoretic myoglobin concentrations in particular are mechanistically linked with an extended dive capacity mobility and modeled myoglobin net surface phenotype, yet little is known regarding the molecular and biochemical underpinnings of this key charge. specialization. We modeled the evolutionary history of this respiratory pigment over 200 million Fig. 3. Inferring maximal myoglobin con- years of mammalian evolution to elucidate the development of maximal diving capacity during the centrations through myoglobin net surface major mammalian land-to-water transitions. charge across the mammalian phylogeny. Methods: We first determined the relationship between maximum myoglobin concentration and its Fig. 4. Details of myoglobin net surface sequence-derived net surface charge across living mammalian taxa. By using ancestral sequence charge evolution in major groups of diving reconstruction, we then traced myoglobin net surface charge across a 130-species phylogeny to mammals. infer ancestral myoglobin muscle concentrations. Last, we estimated maximum dive time in extinct transitional species on the basis of the relationship of this variable with muscle myoglobin concen- Fig. 5. Evolution of myoglobin net surface tration and body mass in extant diving mammals. charge and aquatic habits in Afrotheria. Results: We reveal an adaptive molecular signature of elevated myoglobin net surface charge in Fig. 6. Modeling diving capacity in ancestral all lineages of mammalian divers with an extended aquatic history—from 16-g water shrews to whales, seals, and sea cows. 80,000-kg whales—that correlates with exponential increases in muscle myoglobin concentrations. Integration of this data with body mass predicts 82% of maximal dive-time variation across all SUPPLEMENTARY MATERIALS degrees of diving ability in living mammals. Supplementary Text Discussion: We suggest that the convergent evolution of high myoglobin net surface charge in Figs. S1 to S6 mammalian divers increases intermolecular electrostatic repulsion, permitting higher muscle oxy- Tables S1 to S7 gen storage capacities without potentially deleterious self-association of the protein. Together References with fossil body-mass estimates, our evolutionary reconstruction permits detailed assessments of maximal submergence times and potential foraging ecologies of early transitional ancestors of ADDITIONAL RESOURCES cetaceans, pinnipeds, and sea cows. Our findings support amphibious ancestries for echidnas, talpid video.sciencemag.org/VideoLab/diving/ moles, hyraxes, and elephants, thereby not only establishing the earliest land-to-water transition among placental mammals but also providing a new perspective on the evolution of myoglobin, arguably the best-known protein. Tr ue Beaver Eared Evolutionary recon- Whales seals seals Absolute struction of myoglobin myoglobin Water net surface charge in Muskrat Star- Platypus net surface shrew nosed terrestrial and aquatic charge mole mammals. The figure 5.0 reveals a molecular signa- ture of elevated myoglo- 2.5 bin net surface charge in all lineages of living elite 0.0 mammalian divers with 0 Time (million years ago an extended aquatic his- 50 tory (upper silhouettes). 100 This signature is used Basilosaurus† 150 † Enaliarctos Mammalia here to infer the diving 200 capacity of extinct species Pakicetus† Moeritherium† ) 250 representing stages dur- ing mammalian land-to- water transitions (†). The list of author affiliations is available in the full article online. *Corresponding author. E mail: [email protected] www.sciencemag.org SCIENCE VOL 340 14 JUNE 2013 1303 Published by AAAS RESEARCH ARTICLE centrations in aquatic relative to terrestrial mam mals, consistent with much higher expression yields of sperm whale Mb in Escherichia coli Evolution of Mammalian Diving compared with Mbs of terrestrial mammals (15, 16). We show that high [Mb]max values across all Capacity Traced by Myoglobin Net mammals are highly correlated with increased Mb net surface charge (ZMb) obtained by modeling Surface Charge Mb primary structure onto the tertiary structure of the protein and using site specific, conserved ion 1 2 3 1 Scott Mirceta, Anthony V. Signore, Jennifer M. Burns, Andrew R. Cossins, ization constants. By using ancestral sequence 2 1 Kevin L. Campbell, Michael Berenbrink * reconstruction, we traced the evolution of ZMb and hence [Mb]max across the mammalian phy Extended breath-hold endurance enables the exploitation of the aquatic niche by numerous logeny. Combining this with allometric analysis mammalian lineages and is accomplished by elevated body oxygen stores and adaptations of tmax and fossil body mass estimates, we re that promote their economical use. However, little is known regarding the molecular and constructed the evolution of diving capacity across evolutionary underpinnings of the high muscle myoglobin concentration phenotype of divers. the major groups of mammalian divers. We used ancestral sequence reconstruction to trace the evolution of this oxygen-storing protein across a 130-species mammalian phylogeny and reveal an adaptive molecular signature of Results elevated myoglobin net surface charge in diving species that is mechanistically linked with maximal myoglobin concentration. This observation provides insights into the tempo and routes to Mb Net Surface Charge and Maximal enhanced dive capacity evolution within the ancestors of each major mammalian aquatic Muscle Concentration lineage and infers amphibious ancestries of echidnas, moles, hyraxes, and elephants, offering [Mb]max of elite divers may exceed values in ter a fresh perspective on the evolution of this iconic respiratory pigment. restrial mammals by factors of more than 30, reach ing 100 mg/g of wet mass (Fig. 1A) or 133 mg/ml xpert mammalian divers, such as Northern varies greatly among divers for poorly under of water [assuming 75% (weight/weight) muscle elephant seals and sperm whales, are able stood reasons (4, 10, 11). water content]. High [Mb]max in divers is invar Eto hold their breath and actively forage in Myoglobin (Mb) of the sperm whale was the iablylinkedwithanincreaseinZMb,atpH 6.5 the oceans for periods of well over an hour (1, 2). first protein characterized at the atomic level in from around +1 in terrestrial mammals to about Even for less proficient aquatic or amphibious Nobel prize winningwork(12) and is perhaps +5 in elite divers (Fig. 1A). Although intracellular mammals, maximal dive duration defines maxi the best studied of all proteins. Mammalian Mbs muscle pH in diving mammals is unknown, a mal foraging depth, enables the exploitation of are small, 153 amino acid globular proteins whose similar pattern holds for pH 6.0 and 7.0 and new food sources, determines how far polar ma primary to tertiary structures are highly conserved, thus likely holds over the range of physiological pH rine or temperate freshwater species can venture giving rise to eight alpha helices that enclose a values (fig. S1) (17). Our estimates of ZMb close under ice cover, and limits how long they can hydrophobic core containing the oxygen binding ly agree with the electrophoretic mobilities of pu stay submerged for predator evasion (3 5). heme group and simultaneously provide a highly rified Mbs from selected aquatic and terrestrial The fossil record has revealed highly conver polar external surface. Mb is involved in the mammals (Fig. 2, A and B), confirming the re gent changes in body, limb, and tail structures storage and facilitated diffusion of oxygen within liability of modeling ZMb from Mb amino acid accompanying the secondary transitions of mam muscle cells (13). It has a higher oxygen affinity sequence and conserved tertiary structure and site mals to an aquatic habitat (6). Comparative phys than hemoglobin and is little affected by pH and specific ionization constants. Protein solubility is iological analyses of extant divers have further other allosteric effectors. Although these biochem generally lowest around zero net surface charge, illustrated that the attendant reductions in the en ical properties are conserved across terrestrial and increasing toward both higher and lower net sur ergetic costs of underwater locomotion are cou aquatic mammals (14), Mb and its precursor, apo face charges (18). The positive ZMb in elite divers pled with greatly elevated body oxygen stores Mb (without the heme), are more stable against may cause electrostatic repulsion and thereby help and their economical use (4, 7, 8). At the onset of unfolding and aggregate less easily at high con to reduce the tendency of Mb and/or apo Mb to submergence, an enhanced dive response leads to cessation of breathing, reduced heart rate, and peripheral
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