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Myoglobin-Like Aerotaxis Transducers in Archaea and Bacteria

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Myoglobin-Like Aerotaxis Transducers in Archaea and Bacteria letters to nature when no observer was present. Flight activities were recorded for all bees until any bee in reviewing this manuscript. This work was supported by the National Science Foundation, the cohort was identi®ed as a pollen forager. This procedure ensured that tracked bees were The Research Board of the University of Illinois at Urbana-Champaign, the Biotechnology taking orientation ¯ights and were not foragers. Bees for radar tracking were selected on and Biological Sciences Research Council of the United Kingdom, the British Beekeepers' the basis of their ¯ight experience and age. They were captured as they departed from the Association, the European Community Regional Tsetse and Trypanosomiasis Control hive. A queen-marking cage was used to restrain the bee as the transponder was attached to Programme, the Leverhulme Trust and the United Kingdom Department for International the number tag using double-sided foam tape. The bee was then released from the cage at Development Flexibility Fund. E.A.C. was supported by a National Research Service the height of the hive entrance. When the bee returned to the hive-front, the transponder Award from the NIH. was removed before she was permitted to re-enter the hive. Correspondence and requests for materials should be addressed to E.A.C. (e-mail: [email protected]). Radar tracking The radar study site was a ¯at region of farmland (700 m ´ 900 m) at the Institute of Arable Crops Research, Rothamsted (Harpenden, Hertfordshire, UK). It was planted with cereal crops and was surrounded by ¯owering crops, hedges, wooded areas and buildings5. The radar and transponders have been previously described4,5. The transponder worn by the bees consisted of a 16 mm vertical dipole aerial and a Schottky diode. Two sizes were used, ................................................................. 0.8 mg and 12.0 mg. The larger version weighs less than an average pollen or nectar load1. Glass or plastic tubing was attached to the bottom of the transponder so that it could be Myoglobin-like aerotaxis inserted into a small hole drilled into the number tag. This created a base for the transponder, facilitating its attachment to the bee. Tracks were obtained during June and transducers in Archaea and Bacteria July 1997, on days when the sun or blue sky was visible. Five anemometry stations were set up around the study site, and these recorded wind speed and direction once every 10 s. To obtain a single measure of wind magnitude and direction for each bee ¯ight, the mean Shaobin Hou*, Randy W. Larsen², Dmitri Boudko*, Charles W. Riley*, wind vector at the midpoint between the beginning and end of the ¯ight path was obtained Ece Karatan³, Mike Zimmer³, George W. Ordal³ & Maqsudul Alam* by interpolation of the vectors recorded at the anemometry stations, averaged over the ¯ight period. * Department of Microbiology, Snyder Hall 207, 2538 The Mall, University of Hawaii, Honolulu, Hawaii 96822, USA Data analysis ² Department of Chemistry, 2545 The Mall, University of Hawaii, Honolulu, 53 tracks were obtained from orienting bees, and 29 of them met the following criteria for Hawaii 96822, USA analysis: all signals fell within the 700 m radar range and the tracked path started and ³ Department of Biochemistry, University of Illinois, 506 S. Mathews Ave, Urbana, ended at the hive front. An orientation ¯ight was de®ned as a ¯ight that began with Illinois 61801, USA hovering in front of the hive entrance (23 out of 29); of the remaining 6 tracked bees, most were seen again on subsequent ¯ights preceded by hovering. At the end of her tracked .............................................................................................................................................. ¯ight, one bee lost her identi®cation tag and could not be studied further. Hovering is a Haem-containing proteins such as haemoglobin and myoglobin widely accepted indicator of orientation3. Flight speed is equivalent to the mean ground play an essential role in oxygen transport and storage. Com- speed for the ¯ight, and was calculated by averaging the point-to-point speed of the moving bee based on 3-s radar sampling intervals. Track segments > 9 s in duration were parison of the amino-acid sequences of globins from Bacteria and used for this calculation to match ¯ight-speed sampling intervals to wind-speed infor- Eukarya suggests that they share an early common ancestor, even mation. In cases in which a radar track was divided into segments by a missing signal, the though the proteins perform different functions in these two ¯ight-speed measure ignores the time the bee spent in these gaps unless the plotted data kingdoms1±6. Until now, no members of the globin family have indicated that the ¯ight path continued on the same course and speed. Proportion of time spent in gaps was not correlated with age or experience (data not shown), and probably been found in the third kingdom, Archaea. Recent studies of represents short landings on vegetation. The area de®ned by a tracked ¯ight was calculated biological signalling in the Bacteria and Eukarya have revealed a using the minimum convex polygon method of home range analysis12. The x and y new class of haem-containing proteins that serve as sensors7. Until coordinates of each signal were imported into the Antelope spatial analysis software now, no haem-based sensor has been described in the Archaea. package (FTP://www-biolog.ucsd.edu.research/vehrenbury/programs.html). SAS Insti- tute software was used for all other analyses13. All correlation analyses used the Pearson Here we report the ®rst myoglobin-like, haem-containing protein product moment coef®cient14. The data were transformed to satisfy the requirements of in the Archaea, and the ®rst haem-based aerotactic transducer in this parametric test. Non-parametric tests (Spearman correlation) conducted on the the Bacteria (termed HemAT-Hs for the archaeon Halobacterium untransformed data yielded identical results (data not shown). Quadrants around the hive salinarum, and HemAT-Bs for Bacillus subtilis). These proteins were de®ned by the intersection of two perpendicular lines centred at the hive. exhibit spectral properties similar to those of myoglobin and Received 12 August; accepted 10 November 1999. trigger aerotactic responses. 1. Winston, M. L. The Biology of the Honey Bee (Harvard Univ. Press, Cambridge, MA, 1987). When the hemAT-Hs gene was originally cloned, its product was 2. Becker, L. Untersuchungen uÈber das Heim®ndevermoÈgen der Bienen. Z. Vergl. Physiol. 41, 1±25 predicted to be a soluble signal transducer8 (HemAT-Hs was (1958). originally named HtB)8. HemAT-Bs was identi®ed in the B. subtilis 3. Vollbehr, J. Zur Orientierung junger Honigbienen bei ihrem ersten Orientierungs¯ug Zool. Jb. Allg. Zool. Physiol. 79, 33±69 (1975). genome-sequencing project as the product of an open-reading 4. Riley, J. R. et al. Tracking bees with harmonic radar. Nature 379, 29±30 (1996). frame encoding a protein with marked similarities to methyl- 5. Osborne, J. L. et al. A landscape scale study of bumble bee foraging range and constancy, using accepting chemotaxis proteins (MCPs) (HemAT-Bs was previously harmonic radar. J. Appl. Ecol. 36, 519±533 (1999). named YhfV)9. The predicted translation products of the hemAT-Hs 6. Capaldi, E. A. & Dyer, F. C. The role of orientation ¯ights on homing performance in honeybees. J. Exp. Biol. 202, 1655±1666 (1999). and hemAT-Bs genes, comprising 489 and 432 residues, respectively, 7. Collett, T. S. Landmark learning and guidance of insects. Phil. Trans. R. Soc. Lond. B, 337, 295±303 exhibit two striking features: ®rst, their amino termini (residues (1992). 1±184 in HemAT-Hs and 1±175 in HemAT-Bs) display limited 8. Lindauer, M. Angeborne und erlernte Komponenten in der Sonnenorientierung der Bienen. Z. Vergl. homology to myoglobin (Fig. 1a); and, second, residues 222±489 of Physiol. 42, 43±62 (1959). 9. Dyer, F. C. & Dickinson, J. A. How partially experienced bees estimate the sun's course. Proc. Natl. HemAT-Hs and 198±432 of HemAT-Bs are 30% identical to the Acad. Sci. USA 91, 4471±4474 (1994). cytoplasmic signalling domain of Tsr (ref. 10), a MCP from 10. Visscher, P.K. & Seeley, T. D. Foraging strategies of honeybee colonies in a temperate deciduous forest. Escherichia coli (Fig. 1b). Ecology 6, 1790±1801 (1982). 11. Wehner, R. in Handbook of Sensory Physiology (ed. H. Antrum), Volume VII/6c, 287±616 (Springer, The residues absolutely conserved among all globins are the New York, 1981). proximal histidine in the F helix (F8) and phenylalanine in the 12. White, G. C. & Garrott, R. A. Analysis of Wildlife Radio Tracking Data (Academic, New York, 1990). CD region (CD1)11,12. Highly conserved residues include the distal 13. SAS Stat Users Guide 6. 03 Edition (SAS Institute, Cary, North Carolina, 1988). His in the E helix (E7), Phe in the CD4 region and proline at the 14. Zar, J. H. Biostatistical Analysis (Prentice Hall, Upper Saddle River, New Jersey, 1996). 15. Ribbands, C. R. The Behaviour and Social Life of Honeybee. (Bee Research Association, London, 1953). beginning of the C helix (C2). Three of these residues (Pro in C2, Phe in CD1, His in F8) are conserved in both HemAT-Hs and Acknowledgements HemAT-Bs (asterisks in Fig. 1a). These features suggested to us that HemATs may be haem-containing proteins that generate signals in We thank J. Drew, T. Hallam, J.C. Kuehn, C. Mata and J. Strand for ®eld assistance in Illinois, N. Carreck for beekeeping assistance at Rothamsted, S. Aref for help with data response to binding of oxygen. analysis, and F.C. Dyer and the members of the Fahrbach and Robinson laboratories for To identify the prosthetic groups in HemAT-Hs and HemAT-Bs, 540 © 2000 Macmillan Magazines Ltd NATURE | VOL 403 | 3 FEBRUARY 2000 | www.nature.com letters to nature both proteins were expressed in E.
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