Dating Ammonia-Oxidizing Bacteria with Abundant Eukaryotic Fossils

Author:

Liao Tianhua1ORCID,Wang Sishuo1ORCID,Zhang Hao1ORCID,Stüeken Eva E2ORCID,Luo Haiwei134ORCID

Affiliation:

1. Simon F. S. Li Marine Science Laboratory, School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Shatin , Hong Kong SAR

2. School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews , Queen's Terrace, KY16 9TS , UK

3. Earth and Environmental Sciences Programme, The Chinese University of Hong Kong , Shatin , Hong Kong SAR

4. Institute of Environment, Energy and Sustainability, The Chinese University of Hong Kong , Shatin , Hong Kong SAR

Abstract

Abstract Evolution of a complete nitrogen (N) cycle relies on the onset of ammonia oxidation, which aerobically converts ammonia to nitrogen oxides. However, accurate estimation of the antiquity of ammonia-oxidizing bacteria (AOB) remains challenging because AOB-specific fossils are absent and bacterial fossils amenable to calibrate molecular clocks are rare. Leveraging the ancient endosymbiosis of mitochondria and plastid, as well as using state-of-the-art Bayesian sequential dating approach, we obtained a timeline of AOB evolution calibrated largely by eukaryotic fossils. We show that the first AOB evolved in marine Gammaproteobacteria (Gamma-AOB) and emerged between 2.1 and 1.9 billion years ago (Ga), thus postdating the Great Oxidation Event (GOE; 2.4 to 2.32 Ga). To reconcile the sedimentary N isotopic signatures of ammonia oxidation occurring near the GOE, we propose that ammonia oxidation likely occurred at the common ancestor of Gamma-AOB and Gammaproteobacterial methanotrophs, or the actinobacterial/verrucomicrobial methanotrophs which are known to have ammonia oxidation activities. It is also likely that nitrite was transported from the terrestrial habitats where ammonia oxidation by archaea took place. Further, we show that the Gamma-AOB predated the anaerobic ammonia-oxidizing (anammox) bacteria, implying that the emergence of anammox was constrained by the availability of dedicated ammonia oxidizers which produce nitrite to fuel anammox. Our work supports a new hypothesis that N redox cycle involving nitrogen oxides evolved rather late in the ocean.

Funder

Hong Kong Research Grants Council (RGC) General Research Fund

Natural Science Foundation of China

Hong Kong Research Grants Council Area of Excellence Scheme

Guangdong Basic and Applied Basic Research Foundation

China Postdoctoral Science Foundation

Publisher

Oxford University Press (OUP)

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