Evolution of microbial markets.

Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.

Conservative sex and the benefits of transformation in Streptococcus pneumoniae.

Natural transformation has significant effects on bacterial genome evolution, but the evolutionary factors maintaining this mode of bacterial sex remain uncertain. Transformation is hypothesized to have both positive and negative evolutionary effects on bacteria. It can facilitate adaptation by combining beneficial mutations into a single individual, or reduce the mutational load by exposing deleterious alleles to natural selection. Alternatively, it may expose transformed cells to damaged or otherwise mutated environmental DNA and is energetically expensive. Here, we examine the long-term effects of transformation in the naturally competent species Streptococcus pneumoniae by evolving populations of wild-type and competence-deficient strains in chemostats for 1000 generations. Half of these populations were exposed to periodic mild stress to examine context-dependent benefits of transformation. We find that competence reduces fitness gain under benign conditions; however, these costs are reduced in the presence of periodic stress. Using whole genome re-sequencing, we show that competent populations fix fewer new mutations and that competence prevents the emergence of mutators. Our results show that during evolution in benign conditions competence helps maintain genome stability but is evolutionary costly; however, during periods of stress this same conservativism enables cells to retain fitness in the face of new mutations, showing for the first time that the benefits of transformation are context dependent.

Host diversity affects the abundance of the extraradical arbuscular mycorrhizal network.

Arbuscular mycorrhizal fungi (AMF) can form complex networks in the soil that connect different host plants. Previous studies have focused on the effects of these networks on individual hosts and host communities. However, very little is known about how different host species affect the success of the fungal network itself. Given the potentially strong selection pressure against hosts that invest in a fungal network which benefits their competitors, we predict that the presence of multiple host species negatively affects the growth of the extraradical network. We designed an experiment using an in vitro culture approach to investigate the effect of different hosts (carrot, chichory and medicago) on the formation of a common mycelial network. In vitro root cultures, each inoculated with their own fungal network, were grown in a double split plate design with two host compartments and a common central compartment where fungal networks could form. We found that the size of fungal networks differs depending on the social environment of the host. When host species were propagated in a mixed species environment, the fungal abundance was significantly reduced compared to monoculture predictions. Our work demonstrates how host-to-host conflict can influence the abundance of the fungal partner.

Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance.

The root microbiome is composed of an incredibly diverse microbial community that provides services to the plant. A major question in rhizosphere research is how species in root microbiome communities interact with each other and their host. In the nutrient mutualism between host plants and arbuscular mycorrhizal fungi (AMF), competition often leads to certain species dominating host colonization, with the outcome being dependent on environmental conditions. In the past, it has been difficult to quantify the abundance of closely related species and track competitive interactions in different regions of the rhizosphere, specifically within and outside the host. Here, we used an artificial root system (in vitro root organ cultures) to investigate intraradical (within the root) and extraradical (outside the root) competitive interactions between two closely related AMF species, Rhizophagus irregularis and Glomus aggregatum, under different phosphorus availabilities. We found that competitive interactions between AMF species reduced overall fungal abundance. R. irregularis was consistently the most abundant symbiont for both intraradical and extraradical colonization. Competition was the most intense for resources within the host, where both species negatively affected each other's abundance. We found the investment ratio (i.e. extraradical abundance/intraradical abundance) shifted for both species depending on whether competitors were present or not. Phosphorus availability did not change the outcome of these interactions. Our results suggest that studies on competitive interactions should focus on intraradical colonization dynamics and consider how changes in investment ratio are mediated by fungal species interactions.

Ex situ diet influences the bacterial community associated with the skin of red-eyed tree frogs (Agalychnis callidryas).

Amphibians support symbiotic bacterial communities on their skin that protect against a range of infectious pathogens, including the amphibian chytrid fungus. The conditions under which amphibians are maintained in captivity (e.g. diet, substrate, enrichment) in ex situ conservation programmes may affect the composition of the bacterial community. In addition, ex situ amphibian populations may support different bacterial communities in comparison to in situ populations of the same species. This could have implications for the suitability of populations intended for reintroduction, as well as the success of probiotic bacterial inoculations intended to provide amphibians with a bacterial community that resists invasion by the chytrid fungus. We aimed to investigate the effect of a carotenoid-enriched diet on the culturable bacterial community associated with captive red-eyed tree frogs (Agalychnis callidryas) and make comparisons to bacteria isolated from a wild population from the Chiquibul Rainforest in Belize. We successfully showed carotenoid availability influences the overall community composition, species richness and abundance of the bacterial community associated with the skin of captive frogs, with A. callidryas fed a carotenoid-enriched diet supporting a greater species richness and abundance of bacteria than those fed a carotenoid-free diet. Our results suggest that availability of carotenoids in the diet of captive frogs is likely to be beneficial for the bacterial community associated with the skin. We also found wild A. callidryas hosted more than double the number of different bacterial species than captive frogs with very little commonality between species. This suggests frogs in captivity may support a reduced and diverged bacterial community in comparison to wild populations of the same species, which could have particular relevance for ex situ conservation projects.

Does autophagy mediate age-dependent effect of dietary restriction responses in the filamentous fungus Podospora anserina?

Autophagy is a well-conserved catabolic process, involving the degradation of a cell's own components through the lysosomal/vacuolar machinery. Autophagy is typically induced by nutrient starvation and has a role in nutrient recycling, cellular differentiation, degradation and programmed cell death. Another common response in eukaryotes is the extension of lifespan through dietary restriction (DR). We studied a link between DR and autophagy in the filamentous fungus Podospora anserina, a multicellular model organism for ageing studies and mitochondrial deterioration. While both carbon and nitrogen restriction extends lifespan in P. anserina, the size of the effect varied with the amount and type of restricted nutrient. Natural genetic variation for the DR response exists. Whereas a switch to carbon restriction up to halfway through the lifetime resulted in extreme lifespan extension for wild-type P. anserina, all autophagy-deficient strains had a shorter time window in which ageing could be delayed by DR. Under nitrogen limitation, only PaAtg1 and PaAtg8 mediate the effect of lifespan extension; the other autophagy-deficient mutants PaPspA and PaUth1 had a similar response as wild-type. Our results thus show that the ageing process impinges on the DR response and that this at least in part involves the genetic regulation of autophagy.

Competence increases survival during stress in Streptococcus pneumoniae.

Horizontal gene transfer mediated by transformation is of central importance in bacterial evolution. However, numerous questions remain about the maintenance of processes that underlie transformation. Most hypotheses for the benefits of transformation focus on what bacteria might do with DNA, but ignore the important fact that transformation is subsumed within the broader process of competence. Accordingly, the apparent benefits of transformation might rely less on recombination than on other potential benefits associated with the broader suite of traits regulated by competence. We examined the importance of this distinction in the naturally competent species Streptococcus pneumoniae, focusing specifically on predictions of the DNA-for-repair hypothesis. We confirm earlier results in other naturally competent species that transformation protects against DNA-damaging stress. In addition, we show that the stress-protection extends to non-DNA-damaging stress. More important, we find that for some forms of stress transformation is not required for cells to benefit from the induction of competence. This rejects the narrowly defined DNA-for-repair hypotheses and provides the first support for Claverys' hypothesis that competence, but not necessarily transformation, may act as a general process to relieve stress. Our results highlight the need to distinguish benefits of transformation from broader benefits of competence that do not rely on DNA uptake and recombination.

Calorie restriction causes healthy life span extension in the filamentous fungus Podospora anserina.

Although most fungi appear to be immortal, some show systemic senescence within a distinct time frame. Podospora anserina for example shows an irreversible growth arrest within weeks of culturing associated with a destabilization of the mitochondrial genome. Here, we show that calorie restriction (CR), a regimen of under-nutrition without malnutrition, increases not only life span but also forestalls the aging-related decline in fertility. Similar to respiratory chain deficiencies the life span extension is associated with lower levels of intracellular H(2)O(2) measurements and a stabilization of the mitochondrial genome. Unlike respiratory chain deficiencies, CR cultures have a wild-type-like OXPHOS machinery similar to that of well-fed cultures as shown by native electrophoresis of mitochondrial protein complexes. Together, these data indicate that life span extension via CR is fundamentally different from that via respiratory chain mutations: Whereas the latter can be seen as a pathology, the former promotes healthy life span extension and may be an adaptive response.

Fitness trade-offs modify community composition under contrasting disturbance regimes in Pseudomonas fluorescens microcosms.

Disturbance is thought to be a major factor influencing patterns of biodiversity. In addition, disturbance can modify community composition if there are species specific trade-offs between fitness and disturbance tolerance. Here, we examine the role of disturbance on the evolution of coexisting biofilm-forming morphotypes of Pseudomonas fluorescens maintained in spatially structured laboratory microcosms. We identified four heritably stable ecotypes that varied significantly in their competitiveness under different disturbance treatments. Furthermore, we identified significant trade-offs in competitiveness across disturbance treatments for three of four of these ecotypes. These trade-offs modified dominance relationships between strains and thus altered community composition, with a peak of ecotype diversity occurring at intermediate disturbance frequencies.