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Competition–defense trade-offs in the microbial world

T. Thingstad

Published 2022 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

In PNAS, Guillonneau et al. (1) report experiments that demonstrate a rather intricate trade-off in the predator–prey relationship between a bacterium and its protozoan predator. Trade-offs link positive to negative changes in fitness and therefore constrain the paths of evolution as well as the biodiversity, structure, and function of existing food webs. In a hypothetical world where trade-offs do not exist, it would be possible for an organism to become best in “everything,” presumably leading to a drastic reduction in diversity, if not a collapse of entire food webs (Fig. 1). Understanding the mechanisms and magnitudes of tradeoffs is therefore a central issue in contemporary theoretical ecology and evolution. Experimental verification and quantification of trade-offs are, however, often difficult, perhaps leading to a lag in experimental versus theoretical insight. Trade-offs come in many forms: Some are given by the fundamental physical and geometric constraints to life, exemplified by the trade-off between competition for low concentrations of limiting nutrients (e.g., phosphate) in aquatic bacteria, governed by the physics of diffusion and therefore favored by small cell size (2); counteracting defense which is favored by increasing cell size beyond the prey spectrum of their heterotrophic flagellate predators (3). The complexity is illustrated by the existence also of an additional strategy based on reducing size below the prey spectrum (4, 5). Other trade-offs are more a consequence of biological features, exemplified by bacterial need for efficient transporters to sequester the limiting nutrient, but these transporters may also serve as virus attachment sites (6). Modifying optimized transporters to prevent viral attack is then likely to be very costly in nutrient-limited environments. The mechanisms of defense are probably important for how different trade-offs have different consequences. The prokaryote CRISPR (7) defense mechanism against viruses works by recognizing and destroying viral DNA after it has entered the host cell. Like a virus defense program in computers, CRISPR may have a significant cost in running the program but a relatively small additional cost for adding a new recognition sequence. Consequently, CRISPR should have a cost at the species level, shared by all strains with different sets of recognition sequences. In contrast, transporter modification would imply a high cost for creating a new, defensive strain. The two defense mechanisms should therefore be expected to have different consequences for diversification at species and strain levels in prokaryote communities. In the microbial world, life strategies and their trade-offs have evolved over a timespan of something like 4 billion years (8). Adding to this the potentially high abundances and short generation times of some (modern) bacteria, the number of generations through which predator–prey (and virus–host) arms races and their associated trade-offs have evolved must be immense, and the potential for development of sophisticated mechanisms therefore high. Guillonneau et al.’s (1) study addresses a response strategy to phosphorus (P) limitation found in many prokaryotes: the substitution of phospholipids with sulfolipids (9), reducing their requirement for P. Since this only occurs under P limitation, the substitution seems to have a fitness cost, only worth paying when P is a scarce commodity. Both lipid groups are surface-active compounds, and the reduction in P requirement likely comes with the side effect of a change in cell surface properties. Surface charge and hydrophobicity are known to affect predator efficiency (3), and Guillonneau et al. shows that the substitution of phospholipids with sulfolipids actually reduces predator efficiency. Intriguingly, this gives a reversed trade-off that might look like an “egg of Columbus” for a P-limited organism: a prey strategy that simultaneously improves competitive ability and reduces vulnerability to predation. The complication in this case is, however, that the shift in lipids has an opposite effect on prey digestibility: With sulfolipids, the prey bacterium becomes more digestible in the acid environment of the vacuoles, and therefore stimulates predator growth better than the phospholipid variety, suggested by Guillonneau et al. to create a

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