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  • Review Article
  • Published:

Cell death in planktonic, photosynthetic microorganisms

Nature Reviews Microbiology volume 2, pages 643–655 (2004)Cite this article

Key Points

  • Phytoplankton have pivotal roles in regulating aquatic food webs, biogeochemical cycles, and the Earth's climate. Even though steady-state maintenance of a high ratio of production/biomass in the ocean implies that, on average, phytoplankton grow, die and are replaced once per week, there has been a misconception among oceanographers that they are immortal unless killed or eaten by predators.

  • However, over the past decade it has become increasingly apparent that phytoplankton are not immortal. Upon encountering adverse environmental conditions, they often die spontaneously, with cell death by lysis in field populations exceeding 50% of phytoplankton growth.

  • Here, we discuss exogenous and endogenous mechanisms of phytoplankton death, including viral infection and programmed cell death (PCD). We specifically examine the experimental evidence for PCD in phytoplankton and exploring its evolutionary development and ecological impact.

  • Our analysis indicates that prokaryotic phytoplankton, as well as derived, independently evolving eukaryotic lineages, not only possess similar PCD programme that involve caspase activity, but they possess a core set of proteins that are orthologues of metazoan caspases.

  • Although the discovery of eukaryotic cell-death domains, such as genes that encode metacaspases, in the genomes of the α-proteobacteria suggests that they have a bacterial origin, phytoplankton provide a unique and intriguing paradox that does not fit the mitochondrial inheritance paradigm of cell-death genes. Given the cyanobacterial origin of plastids, phytoplankton span the photosynthetic bacteria–eukaryote transition independent of mitochondria.

  • Preservation of cell death-related genes in phytoplankton would seem to provide a mechanism for negative selection pressure, yet their retention and maintenance suggests some sort of ancient, selective advantage. We speculate as to 'why' phytoplankton activate a cell-death programme and propose several testable hypotheses.

Abstract

Phytoplankton evolved in the Archaean oceans more than 2.8 billion years ago and are of crucial importance in regulating aquatic food webs, biogeochemical cycles and the Earth's climate. Until recently, phytoplankton were considered immortal unless killed or eaten by predators. However, over the past decade, it has become clear that these organisms can either be infected by viruses or undergo programmed cell death (PCD) in response to environmental stress, resulting in mortality. Here, we discuss exogenous and endogenous mechanisms of phytoplankton death, specifically examining the experimental evidence for PCD in phytoplankton and exploring its evolutionary development and ecological impact. We consider phytoplankton PCD as an autocatalytic cell-suicide mechanism in which an endogenous biochemical pathway leads to cellular demise with apoptotic morphological changes. Phytoplankton have a core set of proteins that are orthologues of metazoan caspases. It seems that PCD in prokaryotic phytoplankton, and in independently evolving eukaryotic lineages, has deeply rooted origins that were appropriated and transferred to multicellular plants and animals in the past 700 million years of the Earth's history.

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Figure 1: Prolonged darkness induces PCD in the unicellular, eukaryotic phytoplankton, Dunaliella tertiolecta.
Figure 2: Activation of PCD in ageing cells of the filamentous, prokaryotic phytoplankton Trichodesmium sp. IMS101.
Figure 3: Phylogenetic analysis of phytoplankton metacaspases in the larger context of the caspase-family of proteases.
Figure 4: Placement of phytoplankton PCD into an evolutionary context.
Figure 5: Phylogenetic tree of cyanobacterial 16S rRNA gene sequences illustrating a potential scheme of metacaspase inheritance.
Figure 6: A schematic of ecosystem pathways in the sea illustrating the consequences of phytoplankton PCD or viral infection.

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Acknowledgements

We thank members of our laboratory for helpful discussions and apologize to investigators whose work was not mentioned due to space constraints. The work cited from our laboratory was supported by grants from the National Institute of Health (USA), the Center for Environmental Bioinorganic Chemistry (Princeton University, USA) and the National Science Foundation (USA).

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Authors and Affiliations

  1. Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick, 08901, New Jersey, USA

    Kay D. Bidle & Paul G. Falkowski

  2. Department of Geological Sciences, Rutgers University, New Brunswick, 08901, New Jersey, USA

    Paul G. Falkowski

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  1. Kay D. Bidle
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Correspondence to Paul G. Falkowski.

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Supplementary information

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DATABASES

Entrez

Anabaena variabilis ATCC 29413

Chlamydomonas reinhardtii

Chlorobium tepidum TLS

Gloeobacter violaceus PCC 7421

Nostoc punctiforme

Prochlorococcus marinus MIT 9313

Synechococcus sp. PCC 7942

Synechococcus sp. WH 8102

Synechocystis sp. PCC 6803

Thermosynechococcus elongatus BP-1

Trichodesmium erythraeum

FURTHER INFORMATION

Paul G. Falkowski's laboratory

Cyanobacteria Genome Database

Chlamydomonas Resource Centre

Introduction to the Cyanobacteria

Emiliania huxleyi

Prochlorococcus marinus MED4 genome

Prochlorococcus marinus SS120 genome

Freshwater dinoflagellates

Glossary

PHYTOPLANKTON

A diverse polyphyletic group of photosynthetic prokaryotic and eukaryotic microorganisms that float with the currents.

PRIMARY PRODUCTIVITY

The fixation of CO2 into organic sugars through photosynthesis or chemosynthesis. An overwhelming majority (>90%) of marine primary productivity derives from the photosynthetic activity of phytoplankton.

COCCOLITHOPHORID

An abundant and specialized group of phytoplankton, which precipitate calcium carbonate into hard plates, or 'coccoliths', surrounding the cells. The production of coccoliths gives these organisms an important role in the removal of CO2 from oceanic waters and its subsequent long-term burial. Coccolithorphorids are in the Prymnesiophyte class.

PARACASPASES

A family of proteases found in animals and slime moulds that, on the basis of sequence analysis, are orthologous to caspases and metacaspases.

METACASPASES

A family of proteases found in higher plants, unicellular protists, fungi and specialized bacteria that, on the basis of sequence analysis, are orthologous to caspases and paracaspases.

ORTHOLOGUES

Genes in any number of species that are thought to be descended from a single gene in the last common ancestor of those species. Orthologues result from the isolation of allelic forms in different species and only differ by subsequent independent mutations that have occurred after isolation. Orthologue assignments are purely historical and do not involve function.

PHYTOPLANKTON LINEAGES

The 'red' and 'green' phytoplankton lineages are two ancient superfamilies, or clusters of phyla, of eukaryotic phytoplankton that, based on the morphology of chloroplasts and sequence analysis of the genes contained therein, evolved independently after the primary endosymbiotic event with a cyanobacterium.

KIN SELECTION MODEL

A model proposed to explain the genetic evolution of altruistic behaviour. It is based on the idea that the genetic material of the altruist is equal to the same number of shared alleles with related individuals (siblings).

EUPHOTIC ZONE

The upper zone in the ocean (usually 80–200 m), where light penetration is sufficient to support net primary productivity.

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Bidle, K., Falkowski, P. Cell death in planktonic, photosynthetic microorganisms. Nat Rev Microbiol 2, 643–655 (2004). https://doi.org/10.1038/nrmicro956

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