Obligate mutualistic cooperation limits evolvability.

Cooperative mutualisms are widespread and play fundamental roles in many ecosystems. Given that these interactions are often obligate, the Darwinian fitness of the participating individuals is not only determined by the information encoded in their own genomes, but also the traits and capabilities of their corresponding interaction partners. Thus, a major outstanding question is how obligate cooperative mutualisms affect the ability of organisms to adapt evolutionarily to changing environmental conditions. Here we address this issue using a mutualistic cooperation between two auxotrophic genotypes of Escherichia coli that reciprocally exchanged costly amino acids. Amino acid-supplemented monocultures and unsupplemented cocultures were exposed to stepwise increasing concentrations of different antibiotics. This selection experiment reveals that metabolically interdependent bacteria are generally less able to adapt to environmental stress than autonomously growing strains. Moreover, obligate cooperative mutualists frequently regain metabolic autonomy, resulting in a collapse of the mutualistic interaction. Together, our results identify a limited evolvability as a significant evolutionary cost that individuals have to pay when entering into an obligate mutualistic cooperation.

A Molecular Framework for the Embryonic Initiation of Shoot Meristem Stem Cells.

The establishment of pluripotent stem cells is a key event during plant and animal embryogenesis, but the underlying mechanisms remain enigmatic. We show that in the flowering plant Arabidopsis thaliana, expression of the shoot meristem stem cell marker CLV3 becomes detectable in transition stage embryos. Surprisingly, the key regulator of stem cell homeostasis WUSCHEL (WUS) is expressed but dispensable for stem cell initiation. Rather, the WUS paralog WOX2, a regulator of embryo patterning initiated in the zygote, functions in this process by shielding stem cell progenitors from differentiation. WOX2 upregulates HD-ZIP III transcription factors required for shoot identity and balances cytokinin versus auxin hormone pathways, revealing that classical plantlet regeneration procedures recapitulate the natural induction mechanism. Our findings link transcriptional regulation of early embryo patterning to hormonal control of stem cell initiation and suggest that similar strategies have evolved in plant and animal stem cell formation.

Deletion of Proton Gradient Regulation 5 (PGR5) and PGR5-Like 1 (PGRL1) proteins promote sustainable light-driven hydrogen production in Chlamydomonas reinhardtii due to increased PSII activity under sulfur deprivation.

Continuous hydrogen photo-production under sulfur deprivation was studied in the Chlamydomonas reinhardtii pgr5 pgrl1 double mutant and respective single mutants. Under medium light conditions, the pgr5 exhibited the highest performance and produced about eight times more hydrogen than the wild type, making pgr5 one of the most efficient hydrogen producer reported so far. The pgr5 pgrl1 double mutant showed an increased hydrogen burst at the beginning of sulfur deprivation under high light conditions, but in this case the overall amount of hydrogen produced by pgr5 pgrl1 as well as pgr5 was diminished due to photo-inhibition and increased degradation of PSI. In contrast, the pgrl1 was effective in hydrogen production in both high and low light. Blocking photosynthetic electron transfer by DCMU stopped hydrogen production almost completely in the mutant strains, indicating that the main pathway of electrons toward enhanced hydrogen production is via linear electron transport. Indeed, PSII remained more active and stable in the pgr mutant strains as compared to the wild type. Since transition to anaerobiosis was faster and could be maintained due to an increased oxygen consumption capacity, this likely preserves PSII from photo-oxidative damage in the pgr mutants. Hence, we conclude that increased hydrogen production under sulfur deprivation in the pgr5 and pgrl1 mutants is caused by an increased stability of PSII permitting sustainable light-driven hydrogen production in Chlamydomonas reinhardtii.

Evolution in regulatory regions rapidly compensates the cost of nonoptimal codon usage.

The redundant genetic code contains synonymous codons, whose relative frequencies vary among species. Nonoptimal codon usage lowers gene translation efficiency, potentially leading to a fitness cost. This is particularly relevant for horizontal gene transfer, common among bacteria and a key player in antibiotic resistance propagation. By mimicking the horizontal transfer of an antibiotic resistance gene, we established that a nonoptimal codon usage renders Escherichia coli 10-20 times more sensitive to the antibiotic. After 350 generations of experimental evolution under antibiotic selection pressure, this cost was compensated through both in cis changes in the gene promoter and in trans changes in the host bacterial genome, without introducing mutations in the coding sequence of the resistance gene. Further, we have found experimental evidence for convergent molecular adaptive evolution. The high fitness cost of nonoptimal codon usage remains a minor obstacle to gene fixation upon horizontal transfer. Our results highlight the importance of rapid evolution of regulatory mechanisms in the adaptation to new environmental and genetic situations.

Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo.

Axis formation is one of the earliest patterning events in plant and animal embryogenesis. In Arabidopsis, the main axis of the embryo is evident at the asymmetric division of the zygote into a small, embryonic apical cell and a large extraembryonic basal cell. Here we show that the homeobox genes WOX2 and WOX8, which are initially coexpressed in the zygote, act as complementary cell fate regulators in the apical and basal lineage, respectively. Furthermore, WOX8 expression in the basal cell lineage is required for WOX2 expression and normal development of the proembryo, suggesting an inductive mechanism. The identified WOX cascade is required for normal expression of a reporter gene of the auxin efflux carrier PIN1 and for the formation of auxin response maxima in the proembryo. Thus, our results link the spatial separation of WOX transcription factors to localized auxin response and the formation of the main body axis in the embryo.

Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of photosystem II, reduced photosystem I levels, and hypersensitivity to light.

Photosystem II is a large pigment-protein complex catalyzing water oxidation and initiating electron transfer processes across the thylakoid membrane. In addition to large protein subunits, many of which bind redox cofactors, photosystem II particles contain a number of low molecular weight polypeptides whose function is only poorly defined. Here we have investigated the function of one of the smallest polypeptides in photosystem II, PsbJ. Using a reverse genetics approach, we have inactivated the psbJ gene in the tobacco chloroplast genome. We show that, although the PsbJ polypeptide is not principally required for functional photosynthetic electron transport, plants lacking PsbJ are unable to grow photoautotrophically. We provide evidence that this is due to the accumulation of incompletely assembled water-splitting complexes, which in turn causes drastically reduced photosynthetic performance and extreme hypersensitivity to light. Our results suggest a role of PsbJ for the stable assembly of the water-splitting complex of photosystem II and, in addition, support a control of photosystem I accumulation through photosystem II activity.