Supraspecies genetic systems

Abstract

The genetic integration of diverse organisms results in the generation of three types of supraspecies systems of heredity: the metagenome (the set of genetic factors of a microbial community that occupies a certain ecological niche), the symbiogenome (the functionally integrated system of the partners’ symbiotic genes) and the hologenome (the unitary hereditary system of an organism of symbiotic origin). The integrity of a metagenome is based on the cross-regulation and horizontal transfer of genes in the coevolving organisms. In the soil microbial communities, this is accompanied by maintenance of a stable extracellular DNA pool. The formation of a symbiogenome is defined by highly specific signaling interactions between the partners; these interactions are responsible for the development of common metabolic pathways based on specialized cellular and tissue structures. The transition of a symbiogenome into a hologenome is often accompanied by endosymbiotic gene transfer from microsymbionts to their hosts. In symbiotic bacteria, this transition is coupled with the establishment of multicomponent and reducted types of genomes that are characteristic for ecologically obligatory symbionts and genetically obligatory symbionts, as well as rudimentary genomes characteristic for cellular organelles. In addition, the evolution of symbiotic genomes towards a higher stringency of microsymbiont transmission in the host generations proceeded from pseudo-vertical (via the environment) to transembryonic (via host embryos and surrounding tissues) and transovarian (via host germ cells), with the latter culminating in the establishment of cytoplasmic inheritance of cellular organelles. Based on our analysis, we propose a hypothesis for the origins of an endophytic plant symbiogenome on the basis of host intervention in the metagenome of soil bacteria, which is mediated by host involvement in the quorum-sensing auto-regulation in the microbial community.