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Prochlorococcus: Approved for Export Prochlorococcus: Approved for export Zackary I. Johnson1,2 and Yajuan Lin Department of Oceanography, University of Hawaii, Honolulu, HI 96822 he oceans account for approxi- mately half of global carbon fixation (1), but unlike plant- dominated terrestrial en- Tvironments, marine photosynthesis is dominated by single-celled microbes, or phytoplankton. These phytoplankton are the engines that drive marine food webs and biogeochemistry. Among the vast variety of phytoplankton found in the open ocean, the non-nitrogen-fixing cya- nobacterium Prochlorococcus is the most numerically abundant (2). Thus, under- standing the diversity, physiology, and ecology of Prochlorococcus is critical to describing and predicting the biological processes and patterns that originate at Fig. 1. Prochlorococcus is the smallest marine phytoplankton and important to the marine nitrogen the base of the marine food web and cycle. (Left) Scanning electron micrograph of Prochlorococcus (strain MIT9312). (Right) Conceptual their implications for carbon dioxide diagram of the uptake of some major nitrogen compounds by various phytoplankton groups and their contribution to export production. Diatoms and Synechococcus, among other types of phytoplankton, can uptake and climate variability. In this Ϫ use new NO3 and therefore contribute substantially to the draw-down of carbon dioxide from the surface issue of PNAS, Martiny et al. (3) pro- ϩ ocean (and atmosphere). Prochlorococcus was thought to be in a tightly coupled cycle living only on NH4 vide compelling evidence that some and urea, which is supplied directly or indirectly (by bacterioplankton) by micrograzers. However, Martiny Ϫ strains of Prochlorococcus can use ni- et al. (3) provide strong evidence that Prochlorococcus can also use NO and therefore may contribute Ϫ 3 trate (NO3 ), which is the most abun- more substantially to carbon export from surface waters. dant form of fixed nitrogen in the oceans and often limits production, fur- ther expanding the importance of this necessary for nitrate utilization. But welling (e.g., eddies or equatorial re- tiny organism. other, larger types of prokaryotic and gions), or high latitudes. These observa- As the smallest known marine phyto- eukaryotic phytoplankton, including tions suggest that other factors control plankton, Prochlorococcus has a stream- Synechococcus and diatoms, do have this Prochlorococcus growth and biomass in lined genome of roughly 2,000 genes (4), gene and therefore are able to bloom. these areas. These factors may include unlike eukaryotic algae, which can have Although Prochlorococcus establishes both ‘‘bottom-up’’ processes such as the baseline of primary production well over 10,000 genes (5). But the ϩ other nutrient limitation (non-nitrogen), driven by recycled NH and urea, only tradeoff for this simple complement of 4 Ϫ allelopathic interactions from other mi- genes is a reduced metabolic potential, the phytoplankton that can use NO3 crobes, or competition from faster grow- Ϫ limiting the ability to use some nitrogen such as diatoms can respond to the ing NO3 -using phytoplankton (e.g., Syn- compounds. Nevertheless, Prochlorococ- pulses of high-nitrogen waters, ensuring echococcus, diatoms) and ‘‘top-down’’ cus dominates in most tropical and that they can take advantage of these processes such as tightly controlled graz- subtropical open ocean environments nitrogen oases. ing by their protistan predators. Evi- because its small diameter and large sur- However, Martiny et al. (3) use an dence from nutrient addition experi- face area to volume ratio affords a com- array of metagenomic sequence data ments suggests that Prochlorococcus petitive advantage for the limited light from the Global Ocean Survey (6) rep- populations are tightly regulated by and nutrient resources (Fig. 1 Left). The resenting many different oceanographic grazers, but there is support for bot- nitrogen requirement for this growth is regions, to provide the first evidence tom-up regulation of these populations as largely supplied by urea [(NH2)2CO] that some types of Prochlorococcus may ϩ well (7). Interestingly, Synechococcus, and ammonium (NH4 ), which in turn contain the nitrate reductase gene which is a close cyanobacterial cousin of are largely generated either directly or (narB). Using field RNA samples, they Ϫ Prochlorococcus, utilizes NO3 and does indirectly (mediated by bacterioplank- further demonstrate that this putative bloom in some of these regions. Al- ton) by the small protozoa grazers that Prochlorococcus gene is expressed, though Synechococcus and Prochlorococ- feed on Prochlorococcus. Thus the strongly suggesting that Prochlorococcus Ϫ cus have many similarities in their ge- growth of Prochlorococcus is part of a has the ability to use NO3 . Although nomes, cell properties (e.g., size), and preliminary, this finding has two sub- tightly coupled loop dependent on recy- physiologies and therefore have overlap- cled nitrogen (Fig. 1 Right). stantial implications for our understand- In certain areas, ocean currents bring ing of the functioning of the oceans. Ϫ Ϫ new nitrogen in the form of NO3 to the The ability to use NO3 alters our Author contributions: Z.I.J. and Y.L. wrote the paper. upper sunlit waters, stimulating photo- conception of how Prochlorococcus fits The authors declare no conflict of interest. synthesis and primary production. How- into the marine food web and in partic- See companion article onpage 10787. ever, this new nitrogen was thought to ular what limits and regulates its growth. Ϫ 1To whom correspondence should be addressed. E-mail: be unavailable to Prochlorococcus be- Although it may use NO3 , Prochlorococ- [email protected]. cause none of the genome sequences cus does not dominate in oceanic re- Ϫ 2Present address (as of Aug. 1 2009): Duke University Nich- from laboratory strains contain the sin- gions with high NO3 concentrations such olas School of the Environment and Earth Sciences, 135 gle gene (assimilatory nitrate reductase) as coastal upwelling, open ocean up- Duke Marine Lab Road, Beaufort, NC [email protected] 10400–10401 ͉ PNAS ͉ June 30, 2009 ͉ vol. 106 ͉ no. 26 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0905187106 Downloaded by guest on September 27, 2021 COMMENTARY ping habitats (8), something unique ide from the atmosphere into the ocean) With the metagenomic data presented about Prochlorococcus prevents it from was thought to be largely driven by in Martiny et al. (3) there are now two Ϫ flourishing in these high-NO3 waters. large, fast-sinking algae, but more recent compelling and complementary lines of The second implication of this finding evidence suggests that small cells, such evidence that Prochlorococcus can use Ϫ Ϸ is that Prochlorococcus may be more as Prochlorococcus, may be equally im- NO3 (3, 11), yet none of the 50 important in exporting carbon from the portant in this process that is significant strains isolated to date has been shown upper ocean than originally thought. In for the global climate (10). Additive to contain the narB gene. Nevertheless, the tightly coupled growth and grazing tracer experiments have shown that nat- we already know that the genus Prochlo- ϩ rococcus comprises several different ge- cycle driven by NH4 and urea, nutrients ural populations of Prochlorococcus can Ϫ notypes that can differ in their gene and carbon are recycled continuously in take up NO3 and that it significantly the upper ocean (Fig. 1 Right). Although contributes to new production (10). Be- complement and physiology (12) and carbon dioxide is quickly consumed by cause the potential of Prochlorococcus ecologies (13), each exhibiting its own the phytoplankton, this uptake is bal- niche differentiation. Inventories of the anced by losses to grazing and release to known ecological types (or ecotypes) the upper ocean (and atmosphere). Some types of show that the culture collections do not Ϫ account for all of the Prochlorococcus NO can also be involved in this fast 3 found in the oceans (14), and this dis- spinning cycle when microbes convert Prochlorococcus may crepancy is most acute deeper in the NHϩ to NOϪ through a process called 4 3 water column. This depth is exactly Ϫ nitrification. In nutrient-poor regions of contain the nitrate where new NO fluxes are highest and the oceans, approximately half of the 3 Ϫ narB-containing Prochlorococcus would NO3 consumed by phytoplankton is re- reductase gene (narB). be expected to be found. In addition to cycled through this process (9), thus the Ϫ Ϫ targeting isolates of NO -assimilating ability to use NO gives Prochlorococcus 3 3 Ϫ Prochlorococcus from these areas, direct access to another part of this rapidly to use NO3 has only recently been dem- quantification of the contribution of cycling nitrogen pool. But in systems onstrated, its contribution to new and Ϫ Prochlorococcus to new (and export) where new nitrogen (such as NO3 )is export production has not historically production should be pursued. More added, a net export of carbon from the been included in models of open ocean challenging, but equally important, areas surface ocean can occur, if biomass is marine ecosystems (Fig. 1 Right). Incor- of future study will be to determine removed from the surface layers via di- porating this finding into these models what limits Prochlorococcus growth in Ϫ rect sinking or packaging of cells in has the potential to revise and possibly areas of high NO3 and why it does not dense zooplankton fecal pellets. This increase our estimate of the contribution participate in the bloom dynamics char- Ϫ so-called export production (or biologi- of marine photosynthesis to carbon up- acteristic of many other NO3 -using cal pump that draws down carbon diox- take by the oceans. phytoplankton. 1. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) 6. Rusch DB, et al. (2007) The Sorcerer II Global Ocean 11. Casey JR, Lomas MW, Mandecki J, Walker DE (2007) Primary production of the biosphere: Integrating terres- Sampling Expedition: Northwest Atlantic through East- Prochlorococcus contributes to new pro- trial and oceanic components. Science 281:237–240.
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