Examining the Evidence for Regulated and Programmed Cell Death in Cyanobacteria. How Significant Are Different Forms of Cell Death in Cyanobacteria Population Dynamics?

Daniel J Franklin

doi:10.3389/fmicb.2021.633954

Abstract

Cyanobacteria are ancient and versatile members of almost all aquatic food webs. In freshwater ecosystems some cyanobacteria form “bloom” populations containing potent toxins and such blooms are therefore a key focus of study. Bloom populations can be ephemeral, with rapid population declines possible, though the factors causing such declines are generally poorly understood. Cell death could be a significant factor linked to population decline. Broadly, three forms of cell death are currently recognized – accidental, regulated and programmed – and efforts are underway to identify these and standardize the use of cell death terminology, guided by work on better-studied cells. For cyanobacteria, the study of such differing forms of cell death has received little attention, and classifying cell death across the group, and within complex natural populations, is therefore hard and experimentally difficult. The population dynamics of photosynthetic microbes have, in the past, been principally explained through reference to abiotic (“bottom-up”) factors. However, it has become clearer that in general, only a partial linkage exists between abiotic conditions and cyanobacteria population fluctuations in many situations. Instead, a range of biotic interactions both within and between cyanobacteria, and their competitors, pathogens and consumers, can be seen as the major drivers of the observed population fluctuations. Whilst some evolutionary processes may theoretically account for the existence of an intrinsic form of cell death in cyanobacteria, a range of biotic interactions are also likely to frequently cause the ecological incidence of cell death. New theoretical models and single-cell techniques are being developed to illuminate this area. The importance of such work is underlined by both (a) predictions of increasing cyanobacteria dominance due to anthropogenic factors and (b) the realization that influential ecosystem modeling work includes mortality terms with scant foundation, even though such terms can have a very large impact on model predictions. These ideas are explored and a prioritization of research needs is proposed.

Highlights

Long-term observations (Hunter-Cevera et al, 2020) indicate that the majority of cell losses in populations of the ubiquitous picocyanobacteria Synechococcus are due to ecological interactions and in the open ocean, the persistence, as well as the proliferation, of Prochlorococcus is intimately linked to complex biotic interactions with heterotrophic bacteria (Morris et al, 2011; Roth-Rosenberg et al, 2020)
Some marine cyanobacteria, such as Trichodesmium (“sea-sawdust”), are noted for their ability to form blooms in the tropics and subtropics and Trichodesmium population dynamics are thought to involve a form of programmed cell death (PCD) (Berman-Frank et al, 2004)
With respect to the rapid Microcystis population declines that can be observed in nature (Bozarth et al, 2010), as peaks in cyanophage activity can coincide with drastic reductions in Microcystis abundance, infection events appear to be common (Haarke et al, 2016), and highly strainspecific cyanophages can potentially adopt a lysogenic state (Mann and Clokie, 2012; Van Wichelen et al, 2016), the potential links between viral lysis and the biochemical markers associated with PCD (Bidle, 2015) may be the first point of scrutiny in understanding the causes of rapid Microcystis population declines

Summary

Cyanobacteria Cell Death

GROWTH AND LOSS IN AQUATIC PHOTOSYNTHETIC MICROBES: IMPORTANT BIOTIC INTERACTIONS OVERLIE THE ABIOTIC FUNDAMENTALS. Our knowledge of death rates in Prochlorococcus, which can be shown by inference to be sizable, be it by viral infection, predation, or “spontaneous cell death” is in its infancy (Biller et al, 2014). Some marine cyanobacteria, such as Trichodesmium (“sea-sawdust”), are noted for their ability to form blooms in the tropics and subtropics and Trichodesmium population dynamics are thought to involve a form of programmed cell death (PCD) (Berman-Frank et al, 2004). The Nomenclature Committee on Cell Death has issued recommendations on the use of the terms accidental, regulated, and PCD and their recognized subvariants (Kroemer et al, 2009; and see Aguilera et al this volume)

POPULATION GROWTH AND LOSS IN FRESHWATER CYANOBACTERIA

Intrinsic Causes

Emission of Volatile Organic Compounds

External Factors

GAPS IN OUR KNOWLEDGE AND PRIORITIES FOR STUDY

CONCLUSION