Genetic individuality and interspecies altruism: modelling symbiogenesis using different types of symbiotic bacteria

Abstract

In this minireview, we address the trade-off between biological altruism (group adaptation result-ing from the ability of an organism to improve the fitness of an associate at the expense of its own fitness) and symbiogenesis — the evolutionary pathway based on genetic integration of non-related species. We address symbiogenesis as a multi-stage process, which involves for-mation of superspecific hereditary systems — functionally integral symbiogenomes (under the facultative partners’ interactions) reorganized into the structurally integral hologenomes (in the obligatory symbioses). The best studied case of symbiogenesis is represented by the evolution of the eukaryotic cell based on transformation of symbiotic bacteria into cellular organelles. This evolution is associated with the deep reduction of microsymbionts’ genomes and with allocation of their genes into the hosts. As a result, microsymbionts lost their Genetic INdividuality (GIN), characterized by an ability to implement DNA- and RNA-based template syntheses required for genome maintenance and expression. Under facultative symbiotic dependence on hosts, the par-tial loss of GIN is due to a “symbiont → host” altruism which in the N2-fixing microbe–plant symbioses results in formation of non-reproducible bacterial forms (e.g., intracellular bacteroids in rhizobia or multiple heterocysts in Nostoc). If micro-symbionts lose their ability of autonomous existence (e.g., in the vertically transmitted intracellular symbionts), they are switched to the “forced altruism” in which the GIN reduction is required for the stable persistence of symbionts in hosts. Therefore, organellogenesis involves the sequential increase of the symbionts’ de-pendency on hosts: conditional → facultative → obligatory → absolute. It is associated with the reorganization of microbes into semi-autonomous cellular components, which may be completely devoid of their own genomes.

The prospects for Symbiogenetics: emergence of superorganismal genomes and reconstruction of cellular evolution (mini-review)

“…Importantly, the irreversible bacteroid differentiation is under dual control of both partners (Tikhonovich et al, 2015), suggesting that hosts operate as mediators in transfer of altruistic impacts within the plant-associated microbial populations. This mediation is compensated by the nitrogen flow from rhizobia to plants, showing that in the nodular N 2 -fixing symbioses, the interspecies altruism is involved (Provorov, 2021).…”

Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns

“…Simulation of population dynamics in symbiotic organisms suggests that individual selection explains readily the evolution of antagonism but not of mutualism ( Wyatt et al., 2013 ), which is sometimes addressed as a side-effect of individual adaptations ( Smith, 1989 ). Specifically, DaS models fail to explain the rhizobia evolution for irreversible differentiation into N 2 -fixing bacteroids, which may be addressed as temporary organelles of plant cells ( Coba de la Peña et al., 2017 ), since the bacteroid operation is considered “altruistic” towards the legume hosts ( Provorov, 2021 ).…”

“…However, Nod + strains supported by individual selection may be represented mostly by non-N 2 -fixing cheaters, which require additional genetic changes to be transformed into N 2 -fixing (Fix + ) mutualists. The relevant selective pressures possibly operate in planta at the level of intra-nodular clones: Fix + genotypes may be supported by group (inter-deme) selection ( Provorov, 2021 ). It favors strains with nif/fix gene derepression propagated due to the active supply of bacteria with the plant photosynthesis products based on their exchange for N 2 fixation products ( Figure 5 ).…”

AGRICULTURAL MICROBIOLOGY AND SYMBIOGENETICS: SYNTHESIS OF CLASSICAL IDEAS AND CONSTRUCTION OF HIGHLY PRODUCTIVE AGROCENOSES (review)

“…Качественно новый этап повышения целостности холобионтов связан с возникновением механизмов регулярной (вертикальной) передачи микро-партнеров при размножении хозяев. Она обычно вызывает генетическую редукцию микроорганизмов, которые преобразуются в наследственные детерминанты эукариот, реализующих стратегию пангенезиса -наследования благоприобретенных признаков (40). Наиболее глубокая интеграция с клеткой-хозяином характерна для ее постоянных органелл -митохондрий и пластид: многие гены органелл были перемещены в ядерные хромосомы (41), вследствие чего сформировались мозаичные по происхождению многокомпонентные геномы эукариот.…”