Structure and Evolution of Streptomyces Interaction Networks in Soil and In Silico

Soil grains harbor an astonishing diversity of Streptomyces strains producing diverse secondary metabolites. However, it is not understood how this genotypic and chemical diversity is ecologically maintained. While secondary metabolites are known to mediate signaling and warfare among strains, no systematic measurement of the resulting interaction networks has been available. We developed a high-throughput platform to measure all pairwise interactions among 64 Streptomyces strains isolated from several individual grains of soil. We acquired more than 10,000 time-lapse movies of colony development of each isolate on media containing compounds produced by each of the other isolates. We observed a rich set of such sender-receiver interactions, including inhibition and promotion of growth and aerial mycelium formation. The probability that two random isolates interact is balanced; it is neither close to zero nor one. The interactions are not random: the distribution of the number of interactions per sender is bimodal and there is enrichment for reciprocity—if strain A inhibits or promotes B, it is likely that B also inhibits or promotes A. Such reciprocity is further enriched in strains derived from the same soil grain, suggesting that it may be a property of coexisting communities. Interactions appear to evolve rapidly: isolates with identical 16S rRNA sequences can have very different interaction patterns. A simple eco-evolutionary model of bacteria interacting through antibiotic production shows how fast evolution of production and resistance can lead to the observed statistical properties of the network. In the model, communities are evolutionarily unstable—they are constantly being invaded by strains with new sets of interactions. This combination of experimental and theoretical observations suggests that diverse Streptomyces communities do not represent a stable ecological state but an intrinsically dynamic eco-evolutionary phenomenon

Collective Evolution of Biological and Physical Systems

In this dissertation, I study the evolution of solidification fronts propagating in undercooled liquids, the evolution of microbial communities through diversification fronts propagating along microbial genomes, the evolution of the universality and optimality of the genetic code, and the emergence of genome biases. I present a new phase-field model of solidification which allows efficient computations in the regime when interface kinetic effects dominate over capillary effects. The asymptotic analysis required to relate the parameters in the phase-field with those of the original sharp interface model is straightforward, and the resultant phase-field model can be used for a wide range of material parameters. I model the competition between homologous recombination and point mutation in microbial genomes, and present evidence for two distinct phases, one uniform, the other genetically diverse. Depending on the specifics of homologous recombination, I find that global sequence divergence can be mediated by fronts propagating along the genome, whose characteristic signature on genome structure is elucidated, and apparently observed in closely related genomes from the Bacillus cereus group. Front propagation provides an emergent, generic mechanism for microbial “speciation,” and suggests a classification of microorganisms on the basis of their propensity to support propagating fronts. I propose that selection on the speed, accuracy and energy efficiency of template-directed synthesis processes such as translation, transcription and replication can lead to the spontaneous emergence of genome biases. Selection on translation leads to codon usage bias; selection on transcription or replication leads to nucleotide composition biases such as the GC content. These biases result from the generic tradeoffs inherent to template-directed synthesis and occur even in the absence of biased mutation or direct selection on the nucleotide composition coming from, say, DNA or mRNA stability. In the case of translation, it is the coevolution between codon usage and tRNA expression levels that creates a fitness landscape that enforces quasi-stable patterns of codon usage. Occasional transitions between patterns are expected, due to genetic drift or hitchhiking of slightly deleterious adjustments of the translational system on other beneficial traits. Then, I show that the above coevolutionary dynamics provides an efficient mechanism for optimization of genetic codes, even if, as the frozen accident theory assumes, every amino acid substitution is lethal at least at some genome sites. This research shows that it is possible to account for the optimality of the code within the framework of translation as a standardized competition between tRNA adaptors. Finally, I investigate the proposition that genetic exchange dominating the early evolution of life naturally leads to a common genetic code for all organisms, while promoting their incredible diversity in all other aspects. I present three possible mechanisms through which HGT brings universality - communal advantage of popular codes, HGT of translational components and HGT of protein coding regions. A possible consequence of the interplay of these mechanisms is the concerted evolution towards optimality of a community of organisms sharing the same genetic code and having compatible translational machineries.U of I OnlyStudent has not yet granted open access permissio

Additional file 1: Figure S1. of Quality filtering of Illumina index reads mitigates sample cross-talk

Average quality score per-base for each read type. Tables S1 and S2: Lists of strains and primers used in this study. (DOCX 450 kb