Oscillations and Chaos in Microbial Food Webs

Analogous to the macroscopic world of plants and animals, microorganisms not only compete with one another, but they may also interact as predators and prey. Theory predicts that population dynamics driven by predator-prey interactions may easily generate oscillations. To test this hypothesis, Gregor Fussmann and co-workers investigated a miniature ecosystem that consisted of two common freshwater microorganisms: the unicellular green alga Chlorella (prey), which was growth-limited by nitrogen, and the rotifer Brachionus (predator), which was feeding on Chlorella. It turned out that the population dynamics of this cc DQ

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Figure 5 Experimental study of the population dynamics of a ciliate feeding on two species of bacteria. Dilution rates were as follows: (a) 0.90 d_1; (b) 0.75 d_1; (c) 0.50 d_1 (line indicates a change to 0.75 d_1); (d-g) replicate experiments with 0.50 d_1 (no sampling took place on days 3, 4, and 7-13 in (f) and (g)); (h-i) replicate experiments with 0.45 d_1. Tetrahymena (predator, horizontal bars), Pedobacter (preferred prey, open circles), Brevundimonas (less-preferred prey, filled circles). Reprinted by permission from Macmillan Publishers Ltd: Nature (Becks L, Hilker FM, Malchow H, JUrgens K, and Arndt H (2005) Experimental demonstration of chaos in a microbial food web. Nature 435: 1226-1229.), Copyright (2005).

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Figure 5 Experimental study of the population dynamics of a ciliate feeding on two species of bacteria. Dilution rates were as follows: (a) 0.90 d_1; (b) 0.75 d_1; (c) 0.50 d_1 (line indicates a change to 0.75 d_1); (d-g) replicate experiments with 0.50 d_1 (no sampling took place on days 3, 4, and 7-13 in (f) and (g)); (h-i) replicate experiments with 0.45 d_1. Tetrahymena (predator, horizontal bars), Pedobacter (preferred prey, open circles), Brevundimonas (less-preferred prey, filled circles). Reprinted by permission from Macmillan Publishers Ltd: Nature (Becks L, Hilker FM, Malchow H, JUrgens K, and Arndt H (2005) Experimental demonstration of chaos in a microbial food web. Nature 435: 1226-1229.), Copyright (2005).

predator-prey system depended on the dilution rate and the nitrogen supply rate to the prey. Either one or both species went extinct, or both species coexisted with stable population densities, or predator and prey both survived with oscillating population densities.

Predator-prey dynamics can get even more complex, if more than two species are involved. This was demonstrated by Lutz Becks and co-workers, who investigated the population dynamics of a three-species system: the ciliate Tetrahymena and two of its prey species, the

bacteria Pedobacter and Brevundimonas. Tetrahymena is a teardrop-shaped ciliate of about 50 mm length that is a common microbial predator in many freshwater habitats. It can maintain stable populations when feeding on either Pedobacter or Brevundimonas. When given a choice, Tetrahymena prefers Pedobacter. Hence, Pedobacter is exposed to higher grazing pressure than Brevundimonas. On the other hand, Pedobacter can outcompete Brevundimonas, when Tetrahymena is not present.

Astonishingly, at least four different types of dynamics were discovered in laboratory experiments with this simple assemblage of three species: (1) One of the prey species goes extinct, while Tetrahymena establishes stable populations with the other prey species (Figure 5a). (2) All three species coexist, each of them maintaining stable populations (Figures 5b and 5c). (3) All three species coexist, but the populations ofpredator and prey oscillate with a constant frequency (Figures 5h and 5i). (4) Chaos arises, where all three species still survive, but populations keep changing in a rather erratic pattern (Figures 5d-5g). Chaos implies that the population densities show aperiodic fluctuations, such that the predictability of the exact population dynamics decreases with time. Which of these four different types of dynamics occurs depends on the growth rates of the species and the dilution rate of the experimental system.

Nonequilibrium dynamics generated by multispecies interactions, as for instance in the rock-scissors-paper game or in chaotic food webs, may facilitate species coexistence, and thereby promote microbial biodiversity. Conversely, these nonequilibrium dynamics may reduce the predictability of population dynamics in microbial communities. The implications for ecosystem functioning are not yet fully understood. Ecosystem functioning in the presence of multispecies interactions has therefore also been studied in large-scale bioreactors inoculated with natural mixtures of microorganisms. Typically, these bioreactors host hundreds of (often unidentified) species, which may exhibit very complex population dynamics. Yet, despite high variability at species level, bioreactors may remain stable in terms of pH, oxygen demand, and biogeochemical process rates. These experiments indicate that highly diverse and dynamic microbial communities can maintain stable ecosystem functioning.

In conclusion, we have reviewed some of the basic mechanisms of microbial population dynamics. Strikingly, even relatively simple systems of only a few species can create complex dynamics in controlled laboratory experiments. Most natural ecosystems host a plethora of microorganisms, consuming a wide variety of different resources in species consortia consisting of numerous potential competitors, prey species, and predator species. Although many microorganisms are still unknown, it is likely that their species interactions can be of astounding complexity. These tiny microorganisms do not only provide valuable model systems for the macroscopic world, but they also drive the major biogeochemical cycles of our planet. There is still a lot to learn about them.

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