Microbes in the Anthropocene: spillover of agriculturally selected bacteria and their impact on natural ecosystems

Soil microbial communities are enormously diverse, with at least millions of species and trillions of genes unknown to science or poorly described. Soil microbial communities are key components of agriculture, for example in provisioning nitrogen and protecting crops from pathogens, providing overall ecosystem services in excess of $1000bn per year. It is important to know how humans are affecting this hidden diversity. Much is known about the negative consequences of agricultural intensification on higher-organisms, but almost nothing is known about how alterations to landscapes affect microbial diversity, distributions and processes. We review what is known about spatial flows of microbes and their response to land use change, and outline nine hypotheses to adva nce research of microbiomes across landscapes. We hypothesise that intensified agriculture selects for certain taxa and genes, which then “spill over” into adjacent unmodified areas and generate a halo of genetic differentiation around agricultural fields. Consequently, the spatial configuration and management intensity of different habitats combines with the dispersal ability of individual taxa to determine the extent of spillover, which can impact the functioning of adjacent unmodified habitats. When land scapes are heterogeneous and dispersal rates are high, this will select for large genomes that allow exploitation of multiple habitats , a process that may be accelerated through horizontal gene transfer. Continued expansion of agriculture will increase genotypic similarity, making microbial community functioning increasingly variable in human - dominated landscapes , potentially also impacting the consistent provisioning of ecosystem services . While the resulting economic costs have not been calculated, it is clear that dispersal dynamics of microbes should be taken into consideration to ensure that ecosystem functioning and services are maintained in agri - ecosystem mosaics

Bacteriophages limit the existence conditions for conjugative plasmids

Bacteriophages are a major cause of bacterial mortality and impose strong selection on natural bacterial populations, yet their effects on the dynamics of conjugative plasmids have rarely been tested. We combined experimental evolution, mathematical modeling, and individual-based simulations to explain how the ecological and population genetics effects of bacteriophages upon bacteria interact to determine the dynamics of conjugative plasmids and their persistence. The ecological effects of bacteriophages on bacteria are predicted to limit the existence conditions for conjugative plasmids, preventing persistence under weak selection for plasmid accessory traits. Experiments showed that phages drove faster extinction of plasmids in environments where the plasmid conferred no benefit, but they also revealed more complex effects of phages on plasmid dynamics under these conditions, specifically, the temporary maintenance of plasmids at fixation followed by rapid loss. We hypothesized that the population genetic effects of bacteriophages, specifically, selection for phage resistance mutations, may have caused this. Further mathematical modeling and individual-based simulations supported our hypothesis, showing that conjugative plasmids may hitchhike with phage resistance mutations in the bacterial chromosome

Parallel changes in gut microbiome composition and function in parallel local adaptation and speciation

The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet, relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we utilize three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification

Maintenance of Microbial Cooperation Mediated by Public Goods in Single- and Multiple-Trait Scenarios

Microbes often form densely populated communities, which favor competitive and cooperative interactions. Cooperation among bacteria often occurs through the production of metabolically costly molecules produced by certain individuals that become available to other neighboring individuals; such molecules are called public goods. This type of cooperation is susceptible to exploitation, since nonproducers of a public good can benefit from it while saving the cost of its production (cheating), gaining a fitness advantage over producers (cooperators). Thus, in mixed cultures, cheaters can increase in frequency in the population, relative to cooperators. Sometimes, and as predicted by simple game-theoretic arguments, such increases in the frequency of cheaters cause loss of the cooperative traits by exhaustion of the public goods, eventually leading to a collapse of the entire population. In other cases, however, both cooperators and cheaters remain in coexistence. This raises the question of how cooperation is maintained in microbial populations. Several strategies to prevent cheating have been studied in the context of a single trait and a unique environmental constraint. In this review, we describe current knowledge on the evolutionary stability of microbial cooperation and discuss recent discoveries describing the mechanisms operating in multiple-trait and multiple-constraint settings. We conclude with a consideration of the consequences of these complex interactions, and we briefly discuss the potential role of social interactions involving multiple traits and multiple environmental constraints in the evolution of specialization and division of labor in microbes.info:eu-repo/semantics/publishedVersio

Making the most of clade selection

Clade selection is unpopular with philosophers who otherwise accept multilevel selection theory. Clades cannot reproduce, and reproduction is widely thought necessary for evolution by natural selection, especially of complex adaptations. Using microbial evolutionary processes as heuristics, I argue contrariwise, that (1) clade growth (proliferation of contained species) substitutes for clade reproduction in the evolution of complex adaptation, (2) clade-level properties favoring persistence – species richness, dispersal, divergence, and possibly intraclade cooperation – are not collapsible into species-level traits, (3) such properties can be maintained by selection on clades, and (4) clade selection extends the explanatory power of the theory of evolution

Neutral Aggregation in Finite Length Genotype space

The advent of modern genome sequencing techniques allows for a more stringent test of the neutrality hypothesis of Darwinian evolution, where all individuals have the same fitness. Using the individual based model of Wright and Fisher, we compute the amplitude of neutral aggregation in the genome space, i.e., the probability of finding two individuals at genetic (hamming) distance k as a function of genome size L, population size N and mutation probability per base \nu. In well mixed populations, we show that for N\nu\textless{}1/L, neutral aggregation is the dominant force and most individuals are found at short genetic distances from each other. For N\nu\textgreater{}1 on the contrary, individuals are randomly dispersed in genome space. The results are extended to geographically dispersed population, where the controlling parameter is shown to be a combination of mutation and migration probability. The theory we develop can be used to test the neutrality hypothesis in various ecological and evolutionary systems

A re-evaluation of M. prototuberculosis

It has been suggested that a group of smooth tubercle bacilli, isolated from patients with tuberculosis and associated with Djibouti, East Africa, along with the seven species and subspecies that are traditional members of the Mycobacterium tuberculosis complex, should be considered a single species. This suggestion is based on the sequence similarity of the16S rRNA and segments of six housekeeping genes. The very concept of bacterial species is now subject to debate, and I follow the lead of Maynard Smith, who, in a review of the bacterial species concept, suggested that using genetic distance to define bacterial species was “arbitrary and of little merit”. If defining a species by sequence diversity alone is controversial, then it is important to carefully examine the recent claim that strains of M. tuberculosis are descendants and members of a much more ancient and large bacterial species called Mycobacterium prototuberculosis. Furthermore, given the importance of M. tuberculosis as a human pathogen and the implications for research, it is important to verify the claim that our remote hominid ancestors may have suffered from tuberculosis and that the tubercle bacilli originated in Africa