Opportunistic pathogens generally face two vastly different environments - within the host and outside host. One mechanism allowing for adaptation to alternating environments is switching between phenotypes (phenotypic plasticity). The opportunistic fish pathogen Flavobacterium columnare can be found from natural waters and from fish farms and it exhibits two reversible colony morphologies; a non-virulent “rough” and a virulent “rhizoid” morphology. As compared to natural waters, fish farms can be considered as extreme environments in terms of available host resources, but also in terms of stress caused by chemical and antibiotic treatments. Fish farms could thus be expected to impose higher selection pressures for coping between the within and outside host environment, and to select for increased phenotypic plasticity. To test these ideas we measured growth parameters of rhizoid and rough colony morphotypes of F. columnare isolates both from natural waters and from disease outbreaks at fish farms in different resource concentrations and temperatures, and tested their virulence with a zebrafish challenge model. We found that the non-virulent “rough” morphotypes had a higher growth rate and lower virulence than the “rhizoid” morphotypes, but only if the isolate was originating from the fish farms. This suggests that phenotypic plasticity between two morphotypes of opportunistic pathogen and their characteristic traits is clearly selected for in fish farms rather than in the natural environment.
Environmental opportunist pathogens are common in nature. Two well known examples are Vibrio cholera in humans and Flavobacteria in fish. Yet studies on epidemiology and evolution of pathogenicity are centred on obligate pathogens. Environmental opportunist pathogens do not require host-to-host contacts for transmission, and spend most of their time in the outside-host environment where their abundance depends on biotic and abiotic conditions. Such environmental bacteria can spontaneously gain and loose virulence factors that are likely to be associated with increased growth potential and energetic costs. Non-obligate pathogens have not tightly coevolved to evade host immune system, and pathogen transmission is likely to be strongly dose-dependent. This leads to a paradox: in the absence of hosts pathogenicity is selected against due to reduced competitive ability and this in turn prevents transmission to hosts. How can environmental opportunistic pathogens exist? We propose that environmental variation is a plausible mechanism explaining transition to more virulent forms.
We present a model which combines a SIR system to environmental virulent and non-virulent bacterial strains. We assume the pathogenic strain is a fast growing whereas the competing strain is a better competitor. This system is associated with bi-stability between two regimes: virulent strain with infections and non-virulent strain with no infections. Starting from a lower density the virulent strain is unable to grow or cause infections in a stable environment. If both bacterial strains are subjected to environmental variation, the virulent strain can overcome between-strain competition and increase in density close to infective dose and cause sporadic outbreaks or persistent infections, and thus gain significant fitness increases. Infective cycles may in turn promote further evolution from environmental opportunism to obligate pathogenicity, especially in the case of persistent infections.
Most theories of the evolution of virulence concentrate on obligatory host-pathogen relationships. Yet, many pathogens are environmental opportunists that can also replicate and interact in the outside-host environment. As the survival of these pathogens can be host-independent, also the transmission-virulence trade-off assumed in obligatory pathogens can be relaxed. This might promote evolution of virulence. In environmental opportunist pathogens, selection in the outside-host environment can influence the evolution of virulence and disease dynamics. There is evidence of a trade-off between capability to invade and live in the host, and the efficiency to use outside-host resources. Therefore environmental opportunist pathogens might be relatively weak outside-host competitors. How are new environmental opportunist pathogens then able to invade? We introduce a novel model that combines density-dependent growth and Lotka-Volterra competition between pathogen and non-pathogenic bacteria in the outside-host environment to SI host-pathogen dynamics. We studied evolution of pathogenicity as the ability for new environmental opportunist pathogens to invade. Parameterization was based on columnaris disease that is a worldwide nuisance of fresh water fishes in fish farms.
New environmental opportunist pathogen is able to invade when host growth and outside-host growth of the pathogen are high enough to compensate lower outside-host competition ability. Also, increase in virulence promotes invasion. Selection could thus favor higher virulence in environmental opportunist diseases as compared to obligatory diseases. Strong outside-host competition on the other hand can drive new environmental opportunist pathogen to extinction. Therefore, situations where ecological constrains, such as competition, are relaxed promote environmental opportunism. Thus multiple outside-host ecological constrains, such as competition, can efficiently limit the emergence of new diseases.
Fluctuating temperature is predicted to select for generalist genotypes that are capable of performing well across a wide range of temperatures. Although theories particularly predict fast fluctuations in selecting for thermal generalists, such experiments are scarce. Our aim was to find out whether fluctuating temperature selects for temperature generalists and test how uniform the temperature induced evolutionary changes are across different bacterial species. We set up a factorial experiment where ten replicate populations of nine different bacterial species were propagated separately either in a constant temperature (30 ºC) or in a rapidly fluctuating temperature (2 h 20 ºC - 2 h 30 ºC - 2 h 40 ºC, mean 30 ºC). After 2.5 months we isolated altogether 720 bacterial clones from experimental populations and measured growth rate and yield (growth efficiency) in three constant temperatures (20, 30 and 40 ºC). Meta-analysis of all of the species over all of the temperatures indicated that clones from the fluctuating temperature treatment had higher overall growth efficiency compared to clones from the constant environment. Moreover, the selection was found to be asymmetric, selecting more profoundly the tolerance of hottest temperatures. Generality of the results across studied species gives a strong support for the theories of evolution of thermal generalism but also indicates that evolutionary consequence of fluctuating temperature is especially strong in hot temperatures where the fitness consequences of increased or decreased heat are much more profound than in cold temperatures.
Climate change scenarios do not only expect elevated temperatures but also increased temperature fluctuations. Environmental fluctuations are suggested to select for low levels of plasticity in fitness that is also hypothesized to increase organisms’ ability to invade novel environments and affect virulence of pathogens. We tested these hypotheses and show that across a range of temperatures, opportunistic bacterial pathogen Serratia marcescens that evolved in fluctuating temperature (daily variation between 24 and 38 °C, mean 31 °C), outperforms strains that evolved in constant temperature (31° C) across all measured temperatures. Their better growth was also evident in novel environments with parasitic viruses and predatory protozoans. However, the strains from fluctuating environment were less virulent to Drosophila melanogaster host. Therefore, whilst supporting the hypothesis that evolution in fluctuating environments is paired with tolerance to several novel environments, our results show that adapting to fluctuating environments can also be costly in terms of reduced virulence. Together these results suggest that thermal fluctuations driven by the climate change could affect not only species thermal tolerance but also species’ invasiveness and virulence.