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An Unusual Amino Acid Substitution Within Hummingbird Cytochrome C Oxidase Alters a Key Proton-Conducting Channel

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An Unusual Amino Acid Substitution Within Hummingbird Cytochrome C Oxidase Alters a Key Proton-Conducting Channel bioRxiv preprint doi: https://doi.org/10.1101/610915; this version posted August 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. An unusual amino acid substitution within hummingbird cytochrome c oxidase alters a key proton-conducting channel Cory D. Dunn a * and Vivek Sharma a,b * a Institute of Biotechnology Helsinki Institute of Life Science University of Helsinki 00014 Helsinki Finland b Department of Physics University of Helsinki 00014 Helsinki Finland * Co-Corresponding Authorship Cory Dunn, Ph.D. Vivek Sharma, Ph.D. P.O. Box 56 P.O. Box 64 University of Helsinki University of Helsinki 00014 Finland 00014 Finland Email: [email protected] Email: [email protected] Phone: +358 50 311 9307 Phone: +358 50 5759 509 bioRxiv preprint doi: https://doi.org/10.1101/610915; this version posted August 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. ABSTRACT are specifically encoded by the mitochondrial genome, suggesting that adaptations required Hummingbirds in flight exhibit the highest for exceptional metabolic performance might be metabolic rate of all vertebrates. The found at this location. Here, we find that all bioenergetic requirements associated with hummingbirds harbor a remarkable change hovering flight raise the possibility of positive within their mitochondrial DNA that appears to selection upon proteins encoded by be required for outstanding metabolic properties hummingbird mitochondrial DNA. Here, we of this organism. Further analysis by have identified a non-conservative change computational simulations suggests that this within the mitochondria-encoded cytochrome c hummingbird substitution alters proton oxidase subunit I (COI) that is fixed within movement across the mitochondrial inner hummingbirds, yet exceedingly rare among membrane. other metazoans. This unusual change can also be identified in several nectarivorous hovering INTRODUCTION insects, hinting at convergent evolution linked to diet or mode of flight over ~800 million years. Hummingbirds are distinguished by their use of We performed atomistic molecular dynamics hovering flight to feed upon nectar and insects, simulations using bovine and hummingbird COI to defend their territories, and to carry out models, thereby bypassing experimental courtship displays (1–3). Their exceptional limitations imposed by the inability to modify mobility demands a prodigious level of mtDNA in a site-specific manner. Intriguingly, mitochondrial ATP synthesis, and indeed, the our findings suggest that COI amino acid metabolic rate of hummingbird flight muscles is position 153 provides control over the hydration exceedingly high (4, 5). Many physiological and and activity of a key proton channel. We discuss cellular features of hummingbirds appear to be potential phenotypic outcomes for the tailored to their extreme metabolism, especially hummingbird that are linked to this intriguing when considering that hummingbirds can be instance of positive selection upon the found within hypoxic environments up to 5000 mitochondrial genome. meters above sea level (6). For example, hemoglobin structure (7) and cellular myoglobin SIGNIFICANCE STATEMENT concentration (8) appear to be adapted to the oxygen delivery needs of hummingbirds. How do organisms adapt to niches and Additionally, the hearts of hummingbirds are environments that require unusual metabolic larger, relative to their body size, than other features? Changes to mitochondrial function are birds and can pump at a rate of more than 1000 expected to be tightly linked to bioenergetic beats per minute (9). Beyond ATP synthesis, the adaptation. Several proteins required for metabolism of these tiny endotherms must also converting food into energy useful for the cell buffer against heat loss (4, 10, 11). At the bioRxiv preprint doi: https://doi.org/10.1101/610915; this version posted August 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. subcellular level, adaptation to the need for RESULTS AND DISCUSSION increased ATP and heat production can be readily visualized, since mitochondria in Hummingbird harbors unusual substitutions within hummingbird flight muscles are highly, perhaps the mitochondria-encoded subunit I of cytochrome c maximally, packed with cristae and are found in oxidase close apposition to capillaries (12, 13). Hummingbirds have an exceptionally long We sought coding changes within mtDNA- lifespan when considering the allometric link encoded genes that might license or kindle the between body mass and longevity (14), but extreme metabolic capabilities of hummingbirds. whether hummingbird lifespan is linked to its Toward this goal, we analyzed bird mtDNA- unusual metabolic prowess is unclear. encoded protein sequences obtained from the NCBI Reference Sequence (RefSeq) database Within the mitochondrial inner membrane, (18). Upon close inspection of protein sequence electrons progress through the electron alignments, we discovered a surprising transport chain (ETC), reach the cytochrome c substitution of serine for alanine at position 153 oxidase (COX) complex, and are then used to of COI in all 15 hummingbird species examined reduce oxygen. Proton movements coupled to (Table S1) (for convenience, we use the amino electron passage through COX contribute to the acid numbering associated with the structurally proton motive force (PMF) used for ATP characterized Bos taurus COI subunit). This production and thermogenesis (15, 16). While change was found in no other birds within our several COX subunits are nucleus-encoded and alignment of 645 Aves COI entries (Figure 1). imported to mitochondria, the core, catalytic Since COI is the most commonly used DNA subunits of COX (subunits COI, COII, and sequence barcode for studying animal ecology COIII) are encoded by mitochondrial DNA and speciation (19, 20), we next analyzed (mtDNA) (17), raising the possibility that additional sequences covering the COI region of positive selection upon the mitochondrial interest that we obtained from the Barcode of genome may have contributed to the remarkable Life Data (BOLD) server (21). Initially, we metabolic properties of hummingbirds. Here, we focused upon sequences from the bird order identify an amino acid substitution in COI that Apodiformes, a taxon encompassing is universal among hummingbirds, yet hummingbirds and swifts. 914 of 915 exceedingly rare among other birds and informative samples annotated as vertebrates. Atomistic molecular dynamics (MD) hummingbird-derived were found to carry an simulations suggest that this substitution affects A153S substitution at position 153 of COI (Table COX function and is likely to contribute to the S2). The remaining sample is mis-annotated as uncommon physiological capabilities of hummingbird, as determined by BLASTN hummingbirds. analysis of its barcode (22). In contrast, all 110 non-hummingbird Apodiformes samples 3 bioRxiv preprint doi: https://doi.org/10.1101/610915; this version posted August 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. harbored the ancestral A153. Extending our barcodes suggested that any substitution at analysis to all informative bird barcodes, only position 153 is not widely shared among 15/36,636 samples (< 0.1%) not annotated as members of these vertebrate genera, in contrast hummingbird or its parental clade diverged to members of the hummingbird family, for from A at position 153. Assuming that these COI which the A153S substitution appears universal. alterations were not the result of sequencing Extending our analysis to metazoans, errors, we found that the identified changes to substitution at A153 remains very rare. Indeed, A153 outside of hummingbirds were not fixed only 146/7942 (< 2%) of informative RefSeq COI within each identified genus (Table S3). No sequences harbor a substitution of A153 with other COI change appears universally encoded any other amino acid (Table S5). by hummingbird mtDNA, and position 153 does not contact a nucleus-encoded subunit, Evidence for convergent evolution toward a polar suggesting the lack of a single compensatory amino acid substitution at position 153 of cytochrome change that would lead to substitution c oxidase subunit I neutrality (23). Codons for alanine and serine are separated by a distance of only one base pair During our analysis of metazoan COI, our alteration, suggesting that sequence-level attention was drawn to the prominent presence constraints do not explain the exceptional nature of A153S, and the similar non-conservative of the non-conservative A153S substitution in substitution A153T, in several bee species. Bees COI. Since A153 is nearly universal among and hummingbirds are nectarivorous, birds, yet appears to be substituted for S in all thermogenic, and take advantage of hummingbirds, the A153S change within energetically expensive hovering flight (1, 24). hummingbird COI is likely to have functional Moreover, bee metabolic rate relative to mass relevance and to be an example of adaptive surpasses even that of hummingbird (25). evolution. Analysis of BOLD samples from hymenopteran families Apidae and
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