Cryptic Oxygen Cycling in Anoxic Marine Zones
Garcia-Robledo, E., Padilla, C.C., Aldunate, M., Stewart, F.J., Ulloa, O., Paulmier, A., Gregori, G., Revsbech, N.P., 2017. Cryptic Oxygen Cycling in Anoxic Marine Zones. Proc. Natl. Acad. Sci. 201619844. doi:10.1073/pnas.1619844114
By Montserrat Aldunate
UdeC’s Laboratory for Microbial Oceanography & Millennium Institute of Oceanography
The oxygen minimum zones (OMZs) in the eastern tropical North and South Pacific (ETNP and ETSP, respectively) and the Arabian Sea are subject to such dramatic decreases in oxygen that they have been redefined as anoxic marine zones (AMZs; Ulloa et al., 2012). These zones also differ from OMZs in nitrite accumulation, which is even greater when oxygen levels fall under nanomolar limits of detection and cannot even be detected by the most advanced sensors (Revsbech et al., 2011). This nitrite is a nitrogen form that is key for microbial production of N2 and N2O during denitrification processes and anaerobic ammonium oxidation (anammox). These processes together represent between 30% and 50% of the recycling of nitrogen inorganic compounds (nitrate, nitrite, and ammonium) into atmospheric N2 (Codispoti et al. 2001). However, nitrite can also be produced and consumed through aerobic nitrification (Dalsgaard et al., 2012; Babbin et al., 2014), which seems to be an active pathway in the AMZs in spite of the absence of oxygen, which may also be the case with heterotrophic respiration, for example (Stewart et al., 2012; Kalvelage et al., 2015). Then, how can nitrification and other anaerobic processes such as heterotrophic respiration persist despite the apparent anoxia?
The study by García-Robledo et al., recently published online in the journal PNAS, shows that the abundant phototroph communities frequently detected in AMZs are responsible for the operation of these anaerobic processes. According to this research, these communities form a secondary chlorophyll maximum (SCM) in the anoxic zone just below the oxycline that is sometimes as big as the surface layer of chlorophyll maximum normally observed in oxic zones. The SCM is thought to be mainly formed by non-cultured lineages of the picocyanobacterium Prochlorococcus, characteristic of AMZs and previously reported in ETNP and ETSP (Lavin et al., 2010). As noted by García-Robledo et al., these picocyanobacteria release important quantities of O2 into the anoxic environment, which is consumed by the microbial aerobic community, keeping O2 levels undetectable through conventional techniques. These results are supported by several analyses of the picoplanktonic community forming the SCM of AMZs in ETNP and ETSP off the shores of Mexico and Peru respectively. The analyses covered the performance of high-resolution O2 profiles with high-sensitivity sensors in AMZs with SCMs and included incubation experiments to determine the metabolic rates of oxygen production/consumption and carbon fixation of the SCM community, using different light intensities and molecular analyses to determine the expression of key genes related to aerobic metabolisms.
Incubation experiments showed that for light intensities like those found in situ, i.e. < 10μmol photons-m-2-s-1, O2 production rates are lower than respiration rates; therefore, the O2 produced is immediately consumed by the microbial community, producing a "cryptic oxygen cycle" (Fig. 1). Evidence indicates that the metabolisms causing this consumption are aerobic respiration and nitrite oxidation. In the case of aerobic respiration, there are two enzymes responsible for producing this reaction: high-oxygen-affinity terminal oxidase (HATO) and low-oxygen-affinity terminal oxidase (LATO). The results show that there is a maximum in the expression of the gene encoding for the HATO enzyme (Fig. 1B), which could mean that aerobic respiration can take place in spite of the absence of oxygen detectable by conventional sensors, due to the fact that this enzyme requires levels of only a few nanomoles of O2 to function.
A maximum in the expression of genes associated with nitrite oxidation can also be observed (nxr; Fig. 1B), as well as a maximum in the percentage of organisms associated with this function, such as the oxidizing nitrite bacteria of the genus Nitrospine (Fig. 1C). Finally, gross O2 production and carbon fixation rates in the SCM were comparable to the reported rates for aerobic (nitrite and ammonium oxidation) and anaerobic (denitrification, anammox and sulfate reduction) processes, suggesting a significant effect of local oxygen photosynthesis on the biogeochemical cycles in the Pacific Ocean AMZs.
