Light-Driven Electron Uptake from Nonfermentative Organic Matter to Expedite Nitrogen Dissimilation by Chemolithotrophic Anammox Consortia

Nonphotosynthetic microorganisms are typically unable
to directly
utilize light energy, but light might change the metabolic pathway
of these bacteria indirectly by forming intermediates such as reactive
oxygen species (ROS). This work investigated the role of light on
nitrogen conversion by anaerobic ammonium oxidation (anammox) consortia.
The results showed that high intensity light (>20000 lx) caused ca. 50% inhibition of anammox activity, and total ROS reached
167% at 60,000 lx. Surprisingly, 200 lx light was found to induce
unexpected promotion of the nitrogen conversion rate, and ultraviolet
light (<420 nm) was identified as the main contributor. Metagenomic
and metatranscriptomic analyses revealed that the gene encoding cytochrome c peroxidase was highly expressed only under 200 lx light. 15N isotope tracing, gene abundance quantification, and external
H2O2 addition experiments showed that photoinduced
trace H2O2 triggered cytochrome c peroxidase expression to take up electrons from extracellular nonfermentative
organics to synthesize NADH and ATP, thereby expediting nitrogen dissimulation
of anammox consortia. External supplying reduced humic acid into a
low-intensity light exposure system would result in a maximal 1.7-fold
increase in the nitrogen conversion rate. These interesting findings
may provide insight into the niche differentiation and widespread
nature of anammox bacteria in natural ecotopes.