Metabolismos alternativos del carbono y del nitrógeno en las picocianobacterias que habitan las zonas marinas anóxicas.

Abstract

Prochlorococcus and Synechococcus are the most abundant free-living photosynthetic microorganisms in the ocean and represent approximately 25% of marine primary productivity. Uncultivated lineages of these picocyanobacteria also thrive in the dimly illuminated (<1% of incident light) and high nutrients upper part of the anoxic marine zones (AMZs), generating a secondary chlorophyll maximum (SCM). The availability of nutrients and the energy required for the assimilation of these nutrients are essential factors controling the growth of phytoplankton. Prochlorococcus have divinyl chlorophyll a and b (Chl a2, Chl b2) as the main photosynthetic pigments, which allows them to be very efficient capturing energy for photosynthesis in deeper zones. However, genomic studies and other studies based on Prochlorococcus growth rates suggests that Prochlorococcus lineages have the potential to use alternative carbon (C) sources, so a complementary heterotrophy cannot be ruled out. This is especially important for AMZ ecotypes, which are likely to esperience prolonged periods without the amount of light needed to perform photosynthesis. On the other hand, unlike the surface, the most common forms of nitrogen (N) in AMZs are nitrate (NO3-) and nitrite (NO2-) with nanomolar and undetectable concentrations of ammonium (NH4+) and urea respectively. Surface picocyanobacteria base their N assimilative metabolism on reduced N sources, however, AMZ Prochlorococcus ecotypes have the genetic potential to use different N forms, including NO3- and NO2-; unusual N sources for most Prochlorococcus ecotypes, but common for Synechococcus. This ability would confer ZMA Prochlorococcus an ecological advantage over Prochlorococcus lineages that do not have the genes necessary to assimilate these nutrients. In this thesis, natural SCM communities and the functional groups composing them were investigated through stable isotopes (13C and 15N natural abundance), flow cytometry, and assimilation rates of several C and N sources. Results demonstrated that SCM picocyanobacteria at AMZ, composed mostly by Prochlorococcus, are very efficient in capturing solar energy and their ability to fix C, and also they are probably assimilating glucose as a complementary source of C during moments of absence of light. In addition, during photosynthesis, the SCM releases oxygen (O2) in waters where O2 is undetectable using the most sensitive sensors, reflecting a tight coupling between the production and consumption of this gas, generating then a cryptic O2 cycle. The rates of gross O2 production and C fixation in the SCM were similar to those reported for the oxidation of NO2-, as well as for anaerobic reduction of NO3- and SO42-, which suggests a significant effect of local oxygenic photosynthesis in the biogeochemical cycles of the Pacific AMZs. In addition, the production of C at the SCM can provide 5-47% and 2-20% of the organic matter supplied to the anoxic waters of the Eastern Tropical North Pacific (ETNP) and the Eastern Tropical South Pacific (ETSP) respectively, where part of it is remineralized by dissimilatory NO3- reduction to NO2- and denitrification. Our results also suggest that AMZ Prochlorococcus ecotypes are using a mixture of reduced and partly oxidized N forms (mostly NO2-) to satisfy their nutritional needs. When NH4+ and urea are available, Prochlorococcus preferably uses these reduced N sources, even though their genomic repertoire allows the use of oxidized N sources. The choice of NH4+ and urea can be explained by the low energy needed to assimilate these nutrients even when NO3- is high, a important factor in the SCM (<1% incident light). In addition, Prochlorococcus O2 production could be stimulating aerobic respiration in the AMZs, thus generating the NH4+ that Prochlorococcus needs, without accumulation of this nutrient in the SCM. Accordingly, AMZ picocyanobacteria might thus represent potential competitors with anammox bacteria for NH4+ and NO2-, with ammonia-oxidizing archaea for NH4+, and with nitrite-oxidizing bacteria for NO2-.