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The Arnon–Buchanan cycle: a retrospective, 1966–2016

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Abstract

For the first decade following its description in 1954, the Calvin–Benson cycle was considered the sole pathway of autotrophic CO2 assimilation. In the early 1960s, experiments with fermentative bacteria uncovered reactions that challenged this concept. Ferredoxin was found to donate electrons directly for the reductive fixation of CO2 into alpha-keto acids via reactions considered irreversible. Thus, pyruvate and alpha-ketoglutarate could be synthesized from CO2, reduced ferredoxin and acetyl-CoA or succinyl-CoA, respectively. This work opened the door to the discovery that reduced ferredoxin could drive the Krebs citric acid cycle in reverse, converting the pathway from its historical role in carbohydrate breakdown to one fixing CO2. Originally uncovered in photosynthetic green sulfur bacteria, the Arnon–Buchanan cycle has since been divorced from light and shown to function in a variety of anaerobic chemoautotrophs. In this retrospective, colleagues who worked on the cycle at its inception in 1966 and those presently working in the field trace its development from a controversial reception to its present-day inclusion in textbooks. This pathway is now well established in major groups of chemoautotrophic bacteria, instead of the Calvin–Benson cycle, and is increasingly referred to as the Arnon–Buchanan cycle. In this retrospective, separate sections have been written by the authors indicated. Bob Buchanan wrote the abstract and the concluding comments.

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Notes

  1. The cycle is also called the reductive carboxylic acid cycle, reverse citric acid cycle, and reverse TCA cycle. However, it is increasingly designated the Arnon-Buchanan cycle, the name used here (Fuchs 2008; Berg et al. 2010; Fuchs 2011).

  2. In this article, the organism currently classified as Chlorobaculum thiosulfatophilum is referred to by its earlier name, Chlorobium thiosulfatophilum.

  3. In writing this article, I have re-examined our original data for the citrate cleavage enzyme in Chlorobium cell extracts. We reported that ATP was added for the formation of 14C-asparate from 14C-isocitrate. Although this was consistent with the operation of the then unknown ATP-citrate lyase, the enzyme was mistakenly referred to as citrate lyase [Table 1, (Evans et al. 1966)]. However, here and in Table 2 of the original publication, the enzyme is referred to as citrate lyase. In writing this article, I have gone back to my laboratory notebook of six decades ago and found that, indeed, ATP was added to the original enzyme assay mixture and, moreover, was required for activity. On the basis of these considerations, I have concluded that the name entered in Tables 1 and 2 of our 1966 paper (citrate lyase) was a misnomer. Had the assays been conducted after 1980 the enzyme should have been designated ATP-citrate lyase (Ivanovsky et al. 1980). Our original assay results are thus consistent with the later observations of these investigators. It is rewarding to see the reconciliation of these data. It was long overdue.

  4. Mike Evans, a co-discoverer of the Arnon–Buchanan citric acid cycle, also obtained his Ph.D. with Elsden.

  5. BBB was pleased to serve as Editor for publication of this interesting article in the Proceedings of the (US) National Academy of Sciences.

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Acknowledgements

BBB wishes to acknowledge the kind gift of the wooden dipper by the late Elena Kondratieva (see “Afterword”). Further, on behalf of the authors he thanks Georg Fichs and Ivan Berg for their help in organizing this retrospective. Ivan also did an excellent job in editing the manuscript. Without him the quality of the article would have been compromised. The authors also acknowledge the contributions of Govindjee and Renjie Tang.

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Authors and Affiliations

  1. Department of Plant & Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA, 94720, USA

    Bob B. Buchanan

  2. Department of Biosciences, University of Oslo, Blindern, Box 1066, 0316, Oslo, Norway

    Reidun Sirevåg

  3. Mikrobiologie, Fakultät für Biologie, Albert-Ludwigs-Universität Freiburg, Schänzlestrasse 1, 79104, Freiburg, Germany

    Georg Fuchs

  4. Department of Microbiology, M.V. Lomonosov Moscow State University, 1/12 Lenin’s Hills, Moscow, Russia, 119991

    Ruslan N. Ivanovsky

  5. Southwest University, Chongqing, 2 Tiansheng Rd, Beibei Qu, Chongqing Shi, 400700, China

    Yasuo Igarashi

  6. Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1–1–1, Bunkyo-ku, Tokyo, 113–8657, Japan

    Masaharu Ishii

  7. Department of Microbiology, The Ohio State University, 484 West 12th Avenue, Columbus, OH, 43210, USA

    F. Robert Tabita

  8. Institute for Molecular Microbiology and Biotechnology, University of Münster, Corrensstr. 3, 48149, Münster, Germany

    Ivan A. Berg

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  1. Bob B. Buchanan
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Correspondence to Bob B. Buchanan.

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This article was invited by Terry M. Bricker for publication in Photosynthesis Research, and it has been edited by Govindjee.

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figure b

Деревянный ковш (derevyannyj kovsh or wooden dipper made of aspen). Memento Elena Kondratieva gave to Bob Buchanan during his 1975 visit to Moscow, Russia, while en route to the 12th International Botanical Congress in Leningrad, U.S.S.R.

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Buchanan, B.B., Sirevåg, R., Fuchs, G. et al. The Arnon–Buchanan cycle: a retrospective, 1966–2016. Photosynth Res 134, 117–131 (2017). https://doi.org/10.1007/s11120-017-0429-0

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