Prochlorococcus, a marine photosynthetic prokaryote of global significance - PubMed (original) (raw)

Review

Prochlorococcus, a marine photosynthetic prokaryote of global significance

F Partensky et al. Microbiol Mol Biol Rev. 1999 Mar.

Abstract

The minute photosynthetic prokaryote Prochlorococcus, which was discovered about 10 years ago, has proven exceptional from several standpoints. Its tiny size (0.5 to 0.7 microm in diameter) makes it the smallest known photosynthetic organism. Its ubiquity within the 40 degrees S to 40 degrees N latitudinal band of oceans and its occurrence at high density from the surface down to depths of 200 m make it presumably the most abundant photosynthetic organism on Earth. Prochlorococcus typically divides once a day in the subsurface layer of oligotrophic areas, where it dominates the photosynthetic biomass. It also possesses a remarkable pigment complement which includes divinyl derivatives of chlorophyll a (Chl a) and Chl b, the so-called Chl a2 and Chl b2, and, in some strains, small amounts of a new type of phycoerythrin. Phylogenetically, Prochlorococcus has also proven fascinating. Recent studies suggest that it evolved from an ancestral cyanobacterium by reducing its cell and genome sizes and by recruiting a protein originally synthesized under conditions of iron depletion to build a reduced antenna system as a replacement for large phycobilisomes. Environmental constraints clearly played a predominant role in Prochlorococcus evolution. Its tiny size is an advantage for its adaptation to nutrient-deprived environments. Furthermore, genetically distinct ecotypes, with different antenna systems and ecophysiological characteristics, are present at depth and in surface waters. This vertical species variation has allowed Prochlorococcus to adapt to the natural light gradient occurring in the upper layer of oceans. The present review critically assesses the basic knowledge acquired about Prochlorococcus both in the ocean and in the laboratory.

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Figures

FIG. 1

First records of the occurrence of Prochlorococcus. (A) Electron microscope photograph of “type II cells” from deep samples of the North Atlantic ocean. Reprinted from reference with permission of the publisher. ce, cell envelope; pb, polyhedral bodies; th, thylakoids. Scale bar, 0.5 μm. (B) Analysis of a pigment extract obtained by normal-phase HPLC showing the “unknown Chl a derivative,” indicated by a star. Reprinted from reference with permission of the publisher.

FIG. 2

Analysis of natural Prochlorococcus populations by flow cytometry. (Top) Side scatter (a function of cell size) plotted against red fluorescence of chlorophyll. (Bottom) Orange fluorescence of phycoerythrin plotted against red fluorescence of chlorophyll. All scales are 4-decades logarithmic from 1 to 10,000 (arbitrary units). (Left) Typical surface-layer sample (45 m, deep Equatorial Pacific, 7°S, 150°W, collected 10 November 94). Synechococcus is easily distinguished from Prochlorococcus by its orange phycoerythrin fluorescence. (Middle) Typical deep sample (105 m deep, Equatorial Pacific, 7°S, 150°W, collected 10 November 94). Synechococcus is virtually absent, and the chlorophyll fluorescence of Prochlorococcus is much higher than near the surface (compare the fluorescence of Prochlorococcus and that of the standard beads). Note also the weak orange fluorescence displayed by Prochlorococcus at this depth. (Right) Example of two Prochlorococcus populations coexisting at the same depth (80 m deep, Mediterranean Sea, 37°5′N, 16°52′E, collected 20 June 1996).

FIG. 3

Locations of some of the available Prochlorococcus strains (see Table 1).

FIG. 4

Electron micrographs of longitudinal and cross sections of Prochlorococcus strain MIT9313 showing tightly appressed thylakoids at the periphery of the cell. Scale bar, 0.1 μm. Unpublished photographs courtesy of C. Ting, J. King, and S. W. Chisholm.

FIG. 5

Vertical distributions from bright and dim Prochlorococcus populations in the subtropical Pacific Ocean off Hawaii. The insert represents the vertical profile of side scatter and red chlorophyll fluorescence of the total Prochlorococcus population measured by flow cytometry. Adapted from reference with permission of the publisher.

FIG. 6

Diagram showing the thylakoid proteins in Prochlorococcus and their putative organization by homology to the photosynthetic apparatus of cyanobacteria. The proteins whose genes have been sequenced partially or totally are shown in dark gray (see Table 3), and those which have been characterized only by immunoblotting (35, 90, 132) are shown in light gray. Although phycoerythrin is present in some strains such as SS120, it is not clear whether it is integrated in phycobilisomes, which, if present, would be very scarce. PS I is probably organized in trimers (35), but only one monomer is shown. The insert shows a detail of the Pcb protein which includes six transmembrane hydrophobic domains. For the electron transport chain, only the cytochrome b6-f complex is shown because the existence of other components (such as NADH dehydrogenase and plastoquinone) has not been demonstrated yet. Other probable components of the photosynthetic apparatus such as cytochrome oxidase or ATP synthase are not shown either, since they are still uncharacterized in Prochlorococcus. Abbreviations: CP, chlorophyll-protein complex; Cyt, cytochrome; OEC, oxygen evolving complex.

FIG. 7

Concentrations Prochlorococcus integrated over the water column throughout the world oceans. Based on data from Table 5.

FIG. 8

Relationship between Prochlorococcus integrated concentrations and surface temperature (A) and surface nitrate concentrations (B). Based on data from Table 5.

FIG. 9

Vertical distributions of Prochlorococcus (A) and Synechococcus (B). Based on data from Table 5.

FIG. 10

Typical vertical distributions of Prochlorococcus and Synechococcus. (A and B) Surface layer maximum. (C and D) Deep maximum. (E and F) Uniform distribution over the euphotic zone. (A and B) North tropical Atlantic, EUMELI3 cruise (129). (A) EU site, off the coast of Mauritania (20°N, 18°W). (B) MESO site (18°N, 21°W). (C) North Atlantic 30°N, 23°W (11). (D) Eastern Mediterranean Sea, 34°N 18°E, MINOS cruise (176). (E) Equatorial Pacific 150°W, 5°S (174). (F) Tropical Pacific 150°W, 16°S (174). (D and F) Prochlorococcus chlorophyll fluorescence was too weak to be detected at the surface.

FIG. 11

Phylogenetic relationship between Prochlorococcus isolates and cyanobacteria inferred from 16S rRNA gene sequences. Reprinted from reference with permission of the publisher.

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Prochlorococcus, a marine photosynthetic prokaryote of global significance - PubMed (original) (raw)