Protistan predation interferes with bacterial long-term adaptation to substrate restriction by selecting for defence morphotypes.

Abstract

Bacteria that are introduced into aquatic habitats face a low substrate environment interspersed with rare productive 'hotspots', as well as high protistan grazing. Whereas the former condition should select for growth performance, the latter should favour traits that reduce predation mortality, such as the formation of large cell aggregates. However, protected morphotypes often convey a growth disadvantage, and bacteria thus face a trade-off between investing in growth or defence traits. We set up an evolutionary experiment with the freshwater isolate Sphingobium sp. strain Z007 that conditionally increases aggregate formation in supernatants from a predator-prey coculture. We hypothesized that low substrate levels would favour growth performance and reduce the aggregated subpopulation, but that the concomitant presence of a flagellate predator might conserve the defence trait. After 26 (1-week) growth cycles either with (P+) or without (P-) predators, bacteria had evolved into strikingly different phenotypes. Strains from P- had low numbers of aggregates and increased growth yield, both at the original rich growth conditions and on various single carbon sources. By contrast, isolates from the P+ treatment formed elevated proportions of defence morphotypes, but exhibited lower growth yield and metabolic versatility. Moreover, the evolved strains from both treatments had lost phenotypic plasticity of aggregate formation. In summary, the (transient) residence of bacteria at oligotrophic conditions may promote a facultative oligotrophic life style, which is advantageous for survival in aquatic habitats. However, the investment in defence against predation mortality may constrain microbial adaptation to the abiotic environment.