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  • Review Article
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Prochlorococcus: the structure and function of collective diversity

Nature Reviews Microbiology volume 13, pages 13–27 (2015)Cite this article

Subjects

Key Points

  • Prochlorococcus is the numerically dominant phototroph in the oceans and is responsible for a notable fraction of global photosynthesis.

  • Prochlorococcus populations contain distinct subgroups with remarkable genetic and physiological diversity, which contributes to their stability, abundance and wide distribution in the oceans.

  • Cells have distinct adaptations to environmental factors such as light intensity, temperature and nutrient levels.

  • Although each individual cell has a small, 'streamlined' genome, collectively, the global Prochlorococcus population (that is, the pan-genome) contains a vast number of different genes.

  • Interactions with phages and heterotrophs have a crucial role in shaping Prochlorococcus physiology and diversity.

  • Prochlorococcus represents a useful model system for understanding microbial ecology.

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.

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Figure 1: The Prochlorococcus habitat.
Figure 2: Phylogenetic and genomic diversity of Prochlorococcus.
Figure 3: The Prochlorococcus federation.
Figure 4: The influence of phage predation on Prochlorococcus gene content, population diversity and physiology.

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Acknowledgements

The authors thank members of the Chisholm laboratory, L. Kelly, O. Cordero and M. Polz for providing helpful comments on the manuscript. The authors also thank J. Waldbauer for carrying out the initial calculations that inspired Figure 1b. S.B., P.B. and S.W.C. were supported by grants from the Gordon and Betty Moore Foundation (grant GBMF495 to S.W.C.) and the National Science Foundation (OCE-1153588, OCE-1356460 and DBI-0424599, the NSF Center for Microbial Oceanography Research and Education). D.L. was supported by the Israel Science Foundation (Morasha grant 1504/06) and the European Research Council (starting grant 203406).

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Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Steven J. Biller, Paul M. Berube & Sallie W. Chisholm

  2. Faculty of Biology, Technion – Israel Institute of Technology, Haifa, 32000, Israel

    Debbie Lindell

  3. Department of Biology, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Sallie W. Chisholm

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  1. Steven J. Biller
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Glossary

Phytoplankton

Free-floating aquatic photosynthetic microorganisms that require sunlight and inorganic nutrients for growth

Euphotic zone

The sunlit upper region of the ocean water column that receives sufficient light energy to sustain photosynthesis. The depth can vary depending on local conditions, but it is generally the upper ∼200 m in oligotrophic waters.

Oligotrophic

A term used to describe an environment with low concentrations of available nutrients.

Ecotypes

Genetically and physiologically differentiated subgroups of a species that occupy a distinct ecological niche.

ITS sequence

(Internal transcribed spacer sequence). A non-functional rRNA sequence located between the 16S and 23S ribosomal RNA genes in bacteria, which is a useful phylogenetic marker.

Clades

Coherent phylogenetic groups of organisms, each of which comprises all the descendents of a single ancestor.

Siderophore

A molecule that can bind iron; it is often used by microorganisms to facilitate the acquisition of iron from the environment.

Oxygen minimum zones

Subsurface ocean regions that are deficient in oxygen owing to poor ventilation and high rates of respiration.

Gyres

Ocean systems bounded by circular rotating winds and currents. The five major ocean gyres are found in the North Atlantic, North Pacific, South Atlantic, South Pacific and Indian Oceans.

Pan-genome

The complete set of genes that is encoded by all the genomes of a defined group of organisms.

Synteny

The conserved ordering of genes along a chromosome.

Paralogous genes

A pair of similar genes that were created by a duplication event.

Effective population size

In population genetics, the size of an idealized population that would be expected to behave in the same manner as the actual population in terms of the effects of selection and genetic drift.

Genetic drift

The change in the frequency of an allele in a population due to chance or random events.

Cyanophages

Phages that infect cyanobacteria.

Lysogenic phages

Bacteriophages that are capable of integrating their genome into the host genome and are replicated along with the cell, without killing it.

Calvin cycle

The biochemical process that converts CO2 into organic carbon.

Reducing power

In redox chemistry, the availability of compounds that can supply electrons.

Axenic

A term used to describe a pure culture of a single organism that is free of any other contaminating organism.

Reactive oxygen species

(ROS). Oxygen-containing compounds, such as H2O2, that readily react with and damage cellular components.

Extracellular membrane vesicles

Small (∼20–200 nm diameter) spherical structures enclosed by a lipid bilayer. In Gram-negative cells, they are thought to be derived from the outer membrane.

Mixotrophic

A term used to describe an organism that can use multiple metabolic modes for acquiring energy or carbon for growth. In the context of this Review, this refers to organisms that can use both CO2 (autotrophy) and organic carbon (heterotrophy).

Autotrophic

A term used to describe an organism that can build complex, energy-containing organic molecules from CO2 using either light or inorganic chemical reactions as an energy source. Prochlorococcus is capable of photoautotrophic growth and uses light energy to turn CO2 into organic carbon via photosynthesis.

Microbial loop

The network of interactions among microorganisms at the base of the marine food web through which carbon and other nutrients move before they are supplied to larger organisms.

Salps

Marine tunicates that consume plankton by filter feeding.

Ocean stratification

The division of the water column into low-density and high-density zones, with a boundary layer (the pycnocline) defined by a gradient of densities across which water will not passively mix. Changes in density that lead to stratification are typically due to differences in temperature and salinity.

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Biller, S., Berube, P., Lindell, D. et al. Prochlorococcus: the structure and function of collective diversity. Nat Rev Microbiol 13, 13–27 (2015). https://doi.org/10.1038/nrmicro3378

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