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Published December 2021 | Submitted + Supplemental Material
Journal Article Open

Evolution of the cytochrome bd oxygen reductase superfamily and the function of CydAA' in Archaea

Abstract

Cytochrome bd-type oxygen reductases (cytbd) belong to one of three enzyme superfamilies that catalyze oxygen reduction to water. They are widely distributed in Bacteria and Archaea, but the full extent of their biochemical diversity is unknown. Here we used phylogenomics to identify three families and several subfamilies within the cytbd superfamily. The core architecture shared by all members of the superfamily consists of four transmembrane helices that bind two active site hemes, which are responsible for oxygen reduction. While previously characterized cytochrome bd-type oxygen reductases use quinol as an electron donor to reduce oxygen, sequence analysis shows that only one of the identified families has a conserved quinol binding site. The other families are missing this feature, suggesting that they use an alternative electron donor. Multiple gene duplication events were identified within the superfamily, resulting in significant evolutionary and structural diversity. The CydAA' cytbd, found exclusively in Archaea, is formed by the co-association of two superfamily paralogs. We heterologously expressed CydAA' from Caldivirga maquilingensis and demonstrated that it performs oxygen reduction with quinol as an electron donor. Strikingly, CydAA' is the first isoform of cytbd containing only b-type hemes shown to be active when isolated from membranes, demonstrating that oxygen reductase activity in this superfamily is not dependent on heme d.

Additional Information

© The Author(s), under exclusive licence to International Society for Microbial Ecology 2021. Received 16 January 2021; Revised 06 May 2021; Accepted 17 May 2021. We would like to thank NIH for funding this research (Grant # R01AI148160, Principle Investigator: Dr Robert Gennis). We were inspired by the work of Phil Hugenholtz and his lab in reconciling protein phylogenies with organismal taxonomy and, we thank them for a very productive discussion session on the evolution of aerobic respiratory enzymes. We thank Hank Yu for his valuable comments on the initial paper and, Daan Speth for helping us by organizing the genome data from GTDB into an easily searchable file. We thank Bijoy Desai, Ambika Nadkarni and Rajashekar Iyer for useful discussions on the best naming scheme for the cytochrome bd superfamily. We would also like to thank Kelly Wrighton, Adrienne Narrowe and Reb Daly from the Wrighton lab at the Colorado State University for allowing us to use some of their metatranscriptomic data to demonstrate the expression of cydAA' in the environment. The authors declare no competing interests.

Attached Files

Submitted - 2021.01.16.426971v1.full.pdf

Supplemental Material - 41396_2021_1019_MOESM10_ESM.zip

Supplemental Material - 41396_2021_1019_MOESM11_ESM.zip

Supplemental Material - 41396_2021_1019_MOESM12_ESM.txt

Supplemental Material - 41396_2021_1019_MOESM13_ESM.txt

Supplemental Material - 41396_2021_1019_MOESM14_ESM.txt

Supplemental Material - 41396_2021_1019_MOESM1_ESM.docx

Supplemental Material - 41396_2021_1019_MOESM2_ESM.xlsx

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Supplemental Material - 41396_2021_1019_MOESM8_ESM.xlsx

Supplemental Material - 41396_2021_1019_MOESM9_ESM.zip

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Additional details

Created:
August 22, 2023
Modified:
October 23, 2023