Molecular analysis of the 16S rRNA genes of sorted bacterioplankton cells with bright-red fluorescence confirmed the flow cytometric identification of cyanobacteria. At the oligotrophic station, only sequences related to high-light-adapted Prochlorococcus
clade II (29
) could be found, whereas at the mesotrophic sampling site, only members of Synechococcus
group A were found (27
Prochlorococcus spp. were very abundant in waters from the equator to 8°N [(3.0 ± 1.6) × 108 cells liter−1] and were later replaced at the northern end of the transect by Synechococcus spp. [(1.0 ± 0.5) × 108 cells liter−1 ]. The clear switching of dominance between these two taxa coincided with a transition from the oligotrophic region, characterized by the primary production of 180 ± 16 mg of C m−2 day−1 (number of samples, 4) to the mesotrophic region with primary production of 330 ± 56 mg of C m−2 day−1 (number of samples, 4) (G. R. C. Morgan and A. P. Rees, personal communication). In the oligotrophic region, Prochlorococcus comprised 96.5% ± 3% of all cyanobacteria, while Synechococcus clearly dominated the mesotrophic region, accounting for 97% ± 5% of all cyanobacteria.
We found that both Prochlorococcus and Synechococcus cells incorporated the precursor at a rate comparable to the rates of average bacterioplankton cells (Fig. ). The mean cellular specific activity of a Prochlorococcus cell was 110% of the activity of an average bacterial cell in the oligotrophic region, while the mean activity of a Synechococcus cell was only 30% of the activity of an average bacterial cell in the mesotrophic region. The methionine turnover rate constants of both cyanobacteria suggested that these might decrease with depth (Fig. ).
FIG. 3. Comparison of [35S]methionine uptake rates of flow-sorted Prochlorococcus and Synechococcus cells with uptake rates of average bacterioplankton cells (a) as well as vertical distributions of cyanobacterial methionine turnover (b) and its comparison with (more ...)
Although both Prochlorococcus
cyanobacteria were able to incorporate dissolved amino acids at close to natural concentrations, the ecological significance of this differed widely between the two cyanobacterial genera (Fig. ). In the mesotrophic region, Synechococcus
consumed on average only 1.5% of the dissolved methionine pool per day, compared to an average 46% daily turnover by the other bacterioplankton; in other words, Synechococcus
was responsible for only 3% of methionine turnover by all bacterioplankton (Fig. ). Conversely, in oligotrophic waters Prochlorococcus
turned over on average 8% of the methionine pool daily, compared to 16% turned over daily by the other bacterioplankton, or 33% of the methionine turnover by all bacterioplankton, showing that it could compete directly with other bacterioplankton populations. The competitive success of Prochlorococcus
was spectacular, since it was able to consume one-third of the amino acid pool and represent one-third of the abundance of the total bacterioplankton community. Considering that the contribution of Prochlorococcus
to total phytoplankton production could be as high as 50% (15
is undoubtedly the key algal species in oceanic oligotrophic ecosystems.
Assuming that in the oligotrophic region Prochlorococcus
contributed about 50% (15
) of the total phytoplankton primary production of 180 mg of C m−2
, and with a 6.6 C/N molar ratio (25
), the Prochlorococcus
population nitrogen demand should be about 1.1 mM N m−2
. The leucine-derived bacterioplankton production was estimated to be 25 ± 9 mg of C m−2
(number of samples, 4) in the photic zone of the oligotrophic region (M. V. Zubkov, unpublished data), to which Prochlorococcus
contributed about 30% or 0.1 mM N m−2
. Therefore, the dissolved amino acids, which are an energetically preferential nitrogen source, were estimated to satisfy about 10% of the Prochlorococcus
requirements for nitrogen, while ammonium may have satisfied the remainder of their nitrogen requirements. By consuming amino acids, Prochlorococcus
deprived other bacteria of an important source of organic nitrogen, forcing the latter to use inorganic nitrogen at a higher energetic cost in the organic-carbon-limited oligotrophic environment.
Such strong competition for nutrients may be the driving force behind a shift of photoheterotrophic bacteria towards photosynthesis (4
). It was reported that the contribution of these bacteria to total photosynthesis rises from about 1% in nutrient-rich regions to 10% in oligotrophic regions (13
The presented results may help to explain the current controversy in balancing the carbon cycle in the oligotrophic central regions of the ocean with low primary production (31
), where community respiration may exceed photosynthesis (8
). The dominance of Prochlorococcus
, which consumes organic as well as inorganic nitrogen pools, may generate about a 30% overestimation of bacterial secondary production and hence of computed organic matter decomposition and respiration in oligotrophic waters.
These findings suggest that the classical clear distinction between auto- and heterotrophic microorganisms in the ocean is actually rather blurred, that, at least in very oligotrophic waters, heterotrophic bacteria can use photosynthesis (3
), and, conversely, that photosynthetic cyanobacteria can take up key nutrients heterotrophically. When modeling oceanic ecosystems, one should be aware that we know little about some of the key players in the microbial food web and that one ought to be cautious about one's conclusions, in particular with respect to the ocean's heterotrophic components.