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Biller, Et Al., 2014. “Prochlorococcus: the Structure and Function Of Nature Reviews Microbiology | AOP, published online 1 December 2014; doi:10.1038/nrmicro3378 REVIEWS Prochlorococcus: the structure and function of collective diversity Steven J. Biller1, Paul M. Berube1, Debbie Lindell2 and Sallie W. Chisholm1,3 Abstract | The marine cyanobacterium Prochlorococcus is the smallest and most abundant photosynthetic organism on Earth. In this Review, we summarize our understanding of the diversity of this remarkable phototroph and describe its role in ocean ecosystems. We discuss the importance of interactions of Prochlorococcus with the physical environment, with phages and with heterotrophs in shaping the ecology and evolution of this group. In light of recent studies, we have come to view Prochlorococcus as a ‘federation’ of diverse cells that sustains its broad distribution, stability and abundance in the oceans via extensive genomic and phenotypic diversity. Thus, it is proving to be a useful model system for elucidating the forces that shape microbial populations and ecosystems. 1 Phytoplankton Since the discovery of Prochlorococcus in 1985 , con- constrained and less variable than many other microbial Free-floating aquatic siderable progress has been made in understanding the habitats (such as the soil), and exhibits gradual changes photosynthetic microorganisms characteristics that make this bacterium unique in the on monthly to annual timescales. that require sunlight and microbial world. It is the smallest (the cell diameter is From the perspective of its microbial inhabitants, the inorganic nutrients for growth 0.5–0.7 μm)2 and most abundant photosynthetic organ- oligotrophic ocean is an extremely dilute environment Euphotic zone ism on the planet, with an estimated global population of in terms of both its chemistry and biology (FIG. 1a). For The sunlit upper region of the ~1027 cells3–5. Prochlorococcus has the smallest genome of example, the average Prochlorococcus bacterium may ocean water column that any free-living phototroph6; some isolates have genomes be hundreds of cell diameters away from another cell receives sufficient light energy as small as 1.65 Mbp, with only ~1,700 genes7. It is the of any type, and even a few cell diameters away from to sustain photosynthesis. The phytoplankton depth can vary depending on only type of marine that uses the divinyl essential nutrients, which are found at picomolar to local conditions, but it is form of chlorophyll a and chlorophyll b to harvest light nanomolar concentrations. By contrast, well-studied generally the upper ~200 m energy8, which causes a slight red shift in its absorption model microorganisms, such as Escherichia coli, tend to in oligotrophic waters. spectra2,9. This unique pigmentation has made it possi- reside in relatively nutrient-rich and densely populated ble to determine that Prochlorococcus accounts for 50% environments, such as the gut. Studies have shown that, of the total chlorophyll in vast stretches of the surface to overcome the challenges associated with their dilute 10,11 1Department of Civil and oceans . Collectively, this cyanobacterium produces environment, some marine microorganisms attach to 3 20 Environmental Engineering, an estimated 4 gigatons of fixed carbon each year , which particles or form close associations with other bac- Massachusetts Institute of is approximately the same net primary productivity as teria21. Although microscale patchiness of some form Technology, Cambridge, global croplands12. may contribute to the survival of Prochlorococcus, direct Massachusetts 02139, USA. Prochlorococcus thrives throughout the euphotic zone evidence to support or reject this hypothesis is lacking. 2Faculty of Biology, oligotrophic 1,13 Technion – Israel Institute of of the tropical and subtropical ocean . Nevertheless, the dilute nature of oligotrophic ecosys- Technology, Haifa 32000, The daily light–dark cycle synchronizes cell division in tems clearly imposes a unique set of selective pressures Israel. Prochlorococcus14 and is an important driver of highly on microbial life. 3Department of Biology, choreographed gene expression patterns throughout Prochlorococcus has several traits that make it well- Massachusetts Institute of 15–19 Technology, Cambridge, the day . The euphotic zone is shaped by continuous suited to this dilute habitat. Compared with other phyto- Massachusetts 02139, USA. macroscale gradients of light, temperature and nutrients plankton, Prochlorococcus has a low phosphorus require- Correspondence to S.J.B., (FIG. 1); both light intensity and temperature are highest ment (it has high C/P and N/P ratios)22–24, partly owing S.W.C. at the surface and decrease with depth, whereas nutri- to its relatively small genome22 and the substitution of e-mails: [email protected]; ent levels are typically low at the surface and gradually sulpholipids for phospholipids in the cell membrane25. Its [email protected] doi:10.1038/nrmicro3378 increase with depth. Although there is fine-scale varia- small size results in a high surface-to-volume ratio that Published online tion within the water column, the physical and chemi- facilitates efficient nutrient acquisition and enhances 1 December 2014 cal environment of the ocean as a whole tends to be light absorption, which, when combined with its unique NATURE REVIEWS | MICROBIOLOGY ADVANCE ONLINE PUBLICATION | 1 © 2014 Macmillan Publishers Limited. All rights reserved REVIEWS a Upper Phage mixed Wind-driven Vesicle Diatom layer mixing Light absorbed 40 cell lengths 447 nm Fe 673 nm 2 cell lengthsPO 3– 4 cell lengths 4 Co <1 cell length Zooplankton 200 m + NH4 Prochlorococcus 200 cell lengths Light Temperature Nutrients 100 cell lengths Heterotroph (such as SAR11) Low High b Culture c Field 1.0 0 HL HL 0.8 50 0.6 Light 100 LL 0.4 Depth (m) LL Growth rate (μ) rate Growth 150 0.2 0 200 100 101 102 103 Low High 3 4 5 6 7 8 9 Light intensity (μmol photon per m2 per s) Light intensity Abundance (log cells per L) d Culture e Field 60 HLII 0.6 40 0.5 HLII 20 0.4 0 HLI 0.3 N latitude HLI -20 Growth rate (μ) rate Growth 0.2 -40 0.1 -60 10 15 20 25 30 80 60 40 20 0 10 25 3 5 7 Temperature (°C) W longitude Surface Abundance temperature (log cells per mm2) (°C) Nature Reviews | Microbiology pigmentation9, make it the most efficient light absorber of deep waters grow optimally at substantially lower light any photosynthetic cell; Prochloroccocus is the only phyto­ intensities (termed low-light (LL)-adapted ecotypes) plankton known to absorb more light than it scatters2. than those isolated from the surface (termed high- Oligotrophic Thus, Prochlorococcus can thrive at lower light intensi- light (HL)-adapted ecotypes) (FIG. 1b), which results in A term used to describe an 9 28–30 environment with low ties than those required by most other phytoplankton niche-partitioning in the water column : HL‑adapted concentrations of available and its populations extend deeper in the water column cells are orders of magnitude more abundant in surface nutrients. than almost any other phototroph26, essentially defining waters31–33 but are outnumbered by LL‑adapted cells the lower boundary of photosynthetic life in the oceans. at the base of the euphotic zone (FIG. 1c). Despite the Ecotypes The ability of Prochlorococcus to occupy the entire complexity of ocean dynamics, these distinct groups of Genetically and physiologically differentiated subgroups of a euphotic zone can be largely explained by its micro­ Prochlorococcus shift in relative abundance in reproduc- 34,35 species that occupy a distinct diversity, as different subgroups are adapted to differ- ible annual cycles , which demonstrates the remark- ecological niche. ent light optima for growth9,27. Strains isolated from able robustness of Prochlorococcus populations. The 2 | ADVANCE ONLINE PUBLICATION www.nature.com/reviews/micro © 2014 Macmillan Publishers Limited. All rights reserved REVIEWS ◀ Figure 1 | The Prochlorococcus habitat. a | Prochlorococcus inhabits the entire Although the initial partitioning of Prochlorococ­ euphotic zone, which is characterized by gradients of light, temperature and nutrients. cus into the broad categories of HL- and LL‑adapted The ocean water column is divided into an upper ‘mixed’ layer (where wind and strains was based solely on phenotype9,27,46, molecular heat-driven turbulence homogenizes the distribution of nutrients and cells) and the phylogenetic analyses have shown that this division is stratified and less turbulent deeper waters, where gradients in nutrients form as a result consistent with the earliest phylogenetic split within the of biogeochemical activity. Light levels decrease exponentially with depth; gradients of 31,37,38,40 temperature and nutrient concentrations are largely similar in the mixed layer, whereas Prochlorococcus lineage . HL‑adapted Prochlo­ temperature decreases, and nutrient concentrations increase, with depth. The rococcus strains form a coherent, monophyletic group oligotrophic ocean represents an extremely dilute environment in terms of organisms that resolves into at least six clades (HLI–HLVI)9,27,31,46, and nutrients. Some key players in oligotrophic marine communities are shown, along whereas the LL‑adapted strains are polyphyletic and par- with the distances between them as estimated from their average concentrations. tition into at least six clades (LLI–LLVII)36,47,48 (FIG. 2a). According to these metrics, each Prochlorococcus bacterium is hundreds of cell Although alternative nomenclature has been proposed, diameters away from other members of its
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