Nickel superoxide dismutase protects nitrogen fixation in Trichodesmium

Abstract

Trichodesmium, a major diazotroph in tropical and subtropical oceans, provides a significant amount of bioavailable nitrogen in oligotrophic oceans. Remarkably, the cyanobacteria carry out nitrogen fixation and photosynthesis simultaneously under high light (HL) conditions. Here, we hypothesize that nickel superoxide dismutase (NiSOD) protects the nitrogen fixation process from oxidative stress generated in photosynthesis under high solar radiation conditions. We found that the variations in nitrogen fixation rates closely corresponded to Ni availability under HL conditions. The expression of NiSOD and two representative photosynthetic proteins also corresponded to variations in both nitrogen fixation rates and Ni availability under HL conditions. Trichodesmium collected in the field had a high Ni quota and elevated SOD activity. The evidence supports the conclusion that NiSOD protects nitrogen fixation in Trichodesmium from oxidative stress. The ability to utilize NiSOD may be a major advantage for Trichodesmium under high solar radiation conditions.

Protection of nitrogenase from photosynthetic O₂ evolution in Trichodesmium: methodological pitfalls and advances over 30 years of research

“…Subsequent laboratory studies came to similar conclusions by varying Ni availability together with light intensity and quality (Ho et al 2013, Rodriguez and Ho 2014Chen et al 2022). Notably, the highest N2 fixation rates were observed under the condition of high Ni availability and high light intensity (Ho et al 2013, Rodriguez and Ho 2014, Chen et al 2022, both characteristic features of the surface oceanic waters where Trichodesmium blooms (Middag et al 2020, Chen et al 2022. Chen et al (2022) also measured the concentrations of two representative photosynthetic proteins, i.e., PsbA (D1) and PsaC (core subunit of PSI).…”

“…The low SOD activity at low Ni concentrations also indicates that in Trichodesmium, there was no mutual replacement between NiSOD and MnSOD, although Mn was available in the growth medium, suggesting that MnSOD may not to be involved in O2 •− removal (Ho 2013). Subsequent laboratory studies came to similar conclusions by varying Ni availability together with light intensity and quality (Ho et al 2013, Rodriguez and Ho 2014Chen et al 2022). Notably, the highest N2 fixation rates were observed under the condition of high Ni availability and high light intensity (Ho et al 2013, Rodriguez and Ho 2014, Chen et al 2022, both characteristic features of the surface oceanic waters where Trichodesmium blooms (Middag et al 2020, Chen et al 2022.…”

“…Trichodesmium contains two SOD genes, sodA and sodN, encoding isoforms containing manganese (MnSOD) and nickel (NiSOD), respectively (Dupont et al 2008). The latter has captured attention over the last years (Ho 2013, Rodriguez and Ho 2014Held et al 2021, Chen et al 2022. The laboratory study by Ho (2013) showed that, under sufficient supply of P and Fe, N2 fixation in Trichodesmium was limited by Ni.…”

“…Notably, the highest N2 fixation rates were observed under the condition of high Ni availability and high light intensity (Ho et al 2013, Rodriguez and Ho 2014, Chen et al 2022, both characteristic features of the surface oceanic waters where Trichodesmium blooms (Middag et al 2020, Chen et al 2022. Chen et al (2022) also measured the concentrations of two representative photosynthetic proteins, i.e., PsbA (D1) and PsaC (core subunit of PSI). These proteins also showed the highest concentrations at high Ni availability and high light intensity, providing further support that NiSOD is crucial for protecting the photosynthetic machinery of Trichodesmium from ROS (Chen et al 2022).…”

“…Chen et al (2022) also measured the concentrations of two representative photosynthetic proteins, i.e., PsbA (D1) and PsaC (core subunit of PSI). These proteins also showed the highest concentrations at high Ni availability and high light intensity, providing further support that NiSOD is crucial for protecting the photosynthetic machinery of Trichodesmium from ROS (Chen et al 2022). A study conducted on Trichodesmium field colonies combining mineralogical and molecular characterisation revealed that NiSOD was significantly more abundant when colonies interacted with mineral particles, where Ni availability may be enhanced (Held et al 2021).…”