High Rate of Uptake of Organic Nitrogen Compounds by Prochlorococcus Cyanobacteria as a Key to Their Dominance in Oligotrophic Oceanic Waters

Abstract

Direct evidence that marine cyanobacteria take up organic nitrogen compounds in situ at high rates is reported. About 33% of the total bacterioplankton turnover of amino acids, determined with a representative [ 35 S]methionine precursor and flow sorting, can be assigned to Prochlorococcus spp. and 3% can be assigned to Synechococcus spp. in the oligotrophic and mesotrophic parts of the Arabian Sea, respectively. This finding may provide a mechanism for Prochlorococcus' competitive dominance over both strictly autotrophic algae and other bacteria in oligotrophic regions sustained by nutrient remineralization via a microbial loop.Oxygenic phototrophic cyanobacteria (6,11,28) have been shown to dominate the tropical and subtropical regions of the world's oceans, thereby changing our conception of oceanic ecosystems. The cyanobacterial genus Prochlorococcus dominates phytoplankton in the central oceanic gyres, while Synechococcus spp. can become very abundant in nutrient-rich tropical regions (20,24). Why these organisms dominate such waters remains to be understood. To explain the ecological success of cyanobacteria in these waters, we propose the hypothesis that in these oceanic ecosystems, where nutrient regeneration within a microbial loop (1, 2) predominates over nitrate production, cyanobacteria can use not only the inorganic nutrients NH 4 ϩ , NO 3 Ϫ , and NO 2 Ϫ (16, 21) but also organic compounds containing reduced nitrogen.Although cyanobacteria are unable to incorporate some organic compounds, e.g., thymidine (10), Synechococcus axenic cultures utilize urea (7, 21) and amino acids (5, 19, 23) at a low rate and even show aminopeptidase activity (18). However, Synechococcus photoheterotrophy has always been considered ecologically unimportant. Current knowledge about Prochloroccocus nutrient assimilation (24) is limited, partly because of the existence of only one axenic Prochloroccocus culture (26). Interestingly, this strain (PCC9511) was isolated in the presence of an amino acid, methionine. It was reported that Prochlorococcus cultures take up NH 4 ϩ but that they cannot utilize NO 3 Ϫ or NO 2 Ϫ ; they can also use urea but not other sources of organic nitrogen (21, 26), although amino acids were not tested as a sole nitrogen source.Genomic data from the draft annotations of the MIT9313 and MED4 strains of Prochlorococcus spp. show that they possess several transporter systems for amino acids, as shown on the Department of Energy Joint Genome Institute website (http://www.jgi.doe.gov); however, a further analysis is necessary for the prediction of possible utilization pathways. The genome of the MED4 strain lacks the nitrate and nitrite reductase genes, a further proof that this strain needs to rely on reduced nitrogen compounds, e.g., NH 4 ϩ , amino acids, etc. In working with laboratory cultures of cyanobacteria, it is very challenging to simulate oceanic oligotrophic conditions and the results of laboratory nutrient addition experiments can be extrapolated only with considerable caution. On the othe...

A global perspective on marine photosynthetic picoeukaryote community structure

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Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea

“…Other Synechococcus proteins involved in nitrogen metabolism that were detected include nitrate and nitrite transporters, cyanate hydratase, and the nitrogen regulatory protein P-II (Table 3 and Supplementary Table S3). Prochlorococcus proteins for urea degradation were not detected even though they are present in the genome, but proteins for ammonium and oligopetide transport were detected (Table 3 and Supplementary Table S2), supporting the previous data suggesting that Synechococcus can grow on a wide range of nitrogen sources, whereas high-light adapted Prochlorococcus strains preferentially use ammonium and organic sources of nitrogen Zubkov et al, 2003).…”

Functional distinctness in the exoproteomes of marine Synechococcus

“…as additional nitrogen sources) as part of a mixotrophic lifestyle. Indeed, picocyanobacteria are known for their ability to acquire amino acids and carbohydrates (Montesinos et al ., 1997; Zubkov et al ., 2003; Mary et al ., 2008; Muñoz‐Marín et al ., 2013) at low nanomolar concentrations, potential products of chitinase or protease activity. It is also possible that these exoenzymes may have a role in eliminating competitors, especially diatoms, because the latter contain chitin in their silica cell wall (Brunner et al ., 2009).…”