What is the role and nature of programmed cell death in phytoplankton ecology?

Abstract

Cell death is a fundamental process in all metazoan organisms. In contrast, the ecological role of cell death in phytoplankton has been sorely neglected: the causes and biochemistry of cell death, and the quantitative significance of cell death in the ecology of phytoplankton populations and in broader biogeochemical cycles, are not well understood. Metazoan cell death is much better described, due to its accepted roles in the regulation of multicellular life. In metazoan cells, an influential paradigm suggests that there are two morphological outcomes of cell death, one caused by an ‘active’ pathway within the cell (so-called ‘programmed cell death’; PCD), and the other from a ‘passive’ externally-driven process (necrosis). Here, we examine the development of this paradigm, and associated concepts, in plant, animal, and microbial life, and discuss the role of cell death amongst the diverse taxa of the phytoplankton. Several recent studies suggest PCD operates in cyanobacteria, chlorophytes, and dinoflagellates. A better understanding of phytoplankton cell death will potentially provide insight into bloom development, intercellular signalling and population regulation. Understanding the role of PCD in phytoplankton life-history will likely come through examination of metabolic differentiation within phytoplankton populations, of which at present there are only isolated reports. Although bacterial metabolic differentiation (e.g. in the formation of biofilms) is well accepted, metabolic differentiation and group selection amongst microalgae are poorly understood, and are ideas which merit greater research effort. If a process similar to metazoan PCD is widespread amongst unicellular algae, then a rethinking of the ecological relationships between and within phytoplankton populations will be necessary. We highlight the semantic difficulties present in this relatively new field of study and make recommendations for future study.