Unusual Plastoquinones in Non-Phototrophic Nitrifying Bacteria

Abstract

Isoprenoid quinones are important compounds in most organisms. They are essential in electron and proton transport in respiratory and photosynthetic electron transport chains, and additional functions include oxidative stress defence. The biologically most relevant quinones are naphthoquinones including menaquinone and benzoquinones including ubiquinone and plastoquinone. They differ in their polar headgroup structures, physicochemical properties, and distribution among organisms. Menaquinone is the most widespread quinone in prokaryotes, ubiquinone occurs only in bacteria of the phylum Pseudomonadota and eukaryotes, and plastoquinone exists in phototrophic Cyanobacteria and plants. We found that chemolithoautotrophic nitrifying bacteria of the genus Nitrospira (phylum Nitrospirota) exclusively possess unusual methyl-plastoquinones with a standard redox potential below that of canonical plastoquinone and ubiquinone but above menaquinone, suggesting functional roles in reverse electron transport, ammonia oxidation, alternative energy metabolisms, and oxidative stress mitigation. This extends the known diversity of quinones and suggests that plastoquinone derivatives are essential in ecologically important, non-phototrophic bacteria.

Keywords: Nitrospira; comammox; methyl‐plastoquinones; nitrification; respiration; reverse electron transport.

FIGURE 1

Characterisation and potential physiological roles of methyl‐PQs in Nitrospira. (A) Mass spectrometry spectra of methyl‐PQ 8:8 from N. inopinata and of canonical plastoquinone 9:9 from Chlorogloeopsis fritschii . The headgroups are highlighted in blue and the additional methyl in green. (B) Voltammograms of N. inopinata and N. moscoviensis cells, representing the methyl‐PQs, and of pure ubiquinone (UQ) and menaquinone (MK) for comparison. (C) Genome‐based model of the membrane‐bound respiratory and reverse electron transport chains in comammox and nitrite‐oxidising Nitrospira. Key nitrification enzymes and respiratory complexes are shown. Black arrows indicate electron transport in respiratory electron transport chains, green arrows the reverse electron transport chain, and blue arrows proton translocation across the cytoplasmic membrane. Dashed contours indicate uncertain function of a protein, and dashed lines indicate uncertain electron transfers. At present, the details of electron flow from nitrite oxidoreductase to complexes III and IV via soluble or membrane‐bound c‐type cytochromes remain uncertain (Lücker et al. ; Mundinger et al. 2019). Complex IV of Nitrospira belongs to the cytochrome bd‐type oxygen reductase superfamily but lacks a quinol binding site and likely uses c‐type cytochromes as alternative electron donors (Lücker et al. ; Murali et al. 2021). ETC, electron transport chain; Cyt., cytochrome; Fd, ferredoxin; NOB, nitrite‐oxidising bacteria; Q quinone; other abbreviations see text.