Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Eukaryote–eukaryote endosymbiosis was responsible for the spread of chloroplast (plastid) organelles. Stability is required for the metabolic and genetic integration that drives the establishment of new organelles, yet the mechanisms that act to stabilize emergent endosymbioses—between two fundamentally selfish biological organisms—are unclear. Theory suggests that enforcement mechanisms, which punish misbehavior, may act to stabilize such interactions by resolving conflict. However, how such mechanisms can emerge in a facultative endosymbiosis has yet to be explored. Here, we propose that endosymbiont–host RNA–RNA interactions, arising from digestion of the endosymbiont population, can result in a cost to host growth for breakdown of the endosymbiosis. Using the model facultative endosymbiosis between Paramecium bursaria and Chlorella spp., we demonstrate that this mechanism is dependent on the host RNA-interference (RNAi) system. We reveal through small RNA (sRNA) sequencing that endosymbiont-derived messenger RNA (mRNA) released upon endosymbiont digestion can be processed by the host RNAi system into 23-nt sRNA. We predict multiple regions of shared sequence identity between endosymbiont and host mRNA, and demonstrate through delivery of synthetic endosymbiont sRNA that exposure to these regions can knock down expression of complementary host genes, resulting in a cost to host growth. This process of host gene knockdown in response to endosymbiont-derived RNA processing by host RNAi factors, which we term “RNAi collisions,” represents a mechanism that can promote stability in a facultative eukaryote–eukaryote endosymbiosis. Specifically, by imposing a cost for breakdown of the endosymbiosis, endosymbiont–host RNA–RNA interactions may drive maintenance of the symbiosis across fluctuating ecological conditions.

Emergent RNA-RNA interactions can promote stability in a nascent phototrophic endosymbiosis

Eukaryote-eukaryote endosymbiosis was responsible for the spread of photosynthetic organelles. Interaction stability is required for the metabolic and genetic integration that drives the establishment of new organelles, yet the mechanisms which act to stabilise nascent endosymbioses - between two fundamentally selfish biological organisms - are unclear. Theory suggests that enforcement mechanisms, which punish misbehaviour, may act to stabilise such interactions by resolving conflict. However, how such mechanisms can emerge in a nascent eukaryote-eukaryote endosymbiosis has yet to be explored. Here, we propose that endosymbiont-host RNA-RNA interactions, arising from digestion of endosymbionts, can result in a cost to host growth for breakdown of the endosymbiosis. Using the model nascent endosymbiosis, Paramecium bursaria - Chlorella spp., we demonstrate that this mechanism is dependent on the host RNA-interference (RNAi) pathway. We reveal through small RNA (sRNA) sequencing that endosymbiont-derived mRNA released upon endosymbiont digestion can be processed by the host RNAi system into 23-nt sRNA. We additionally identify multiple regions of shared sequence identity between endosymbiont and host mRNA, and demonstrate, through delivery of synthetic endosymbiont sRNA, that exposure to these regions can knock-down expression of complementary host genes, resulting in a cost to host growth. This process of host gene knock-down in response to endosymbiont-derived RNA processing by the host, which we term 'RNAi-collisions', represents a mechanism which can promote stability in a nascent eukaryote-eukaryote endosymbiosis. By imposing a cost for breakdown of the endosymbiosis, endosymbiont-host RNA-RNA interactions may drive maintenance of a symbiosis across fluctuating ecologies and symbiotic states.

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

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.

Contrasting multilevel relationships between behavior and body mass in blue tit nestlings

Repeatable behaviors (i.e., animal personality) are pervasive in the animal kingdom and various mechanisms have been proposed to explain their existence. Genetic and nongenetic mechanisms, which can be equally important, predict correlations between behavior and body mass on different levels (e.g., genetic and environmental) of variation. We investigated multilevel relationships between body mass measured on weeks 1, 2, and 3 and three behavioral responses to handling, measured on week 3, which form a behavioral syndrome in wild blue tit nestlings. Using 7 years of data and quantitative genetic models, we find that all behaviors and body mass on week 3 are heritable (h2 = 0.18–0.23) and genetically correlated, whereas earlier body masses are not heritable. We also find evidence for environmental correlations between body masses and behaviors. Interestingly, these environmental correlations have different signs for early and late body masses. Altogether, these findings indicate genetic integration between body mass and behavior and illustrate the impacts of early environmental factors and environmentally mediated growth trajectory on behaviors expressed later in life. This study, therefore, suggests that the relationship between personality and body mass in developing individuals is due to various underlying mechanisms, which can have opposing effects. Future research on the link between behavior and body mass would benefit from considering these multiple mechanisms simultaneously.

The virus integrations in gut microbes associated with dysbiosis of microbial community in tumorigenesis of colorectal carcinoma

Patients with colorectal cancer (CRC) have a different gut microbial and viral communities from healthy individuals. But little is known about the ways and functions of interaction of virus-bacteria, let alone its correlation with the aetiology of CRC. In this study we aimed to identify the association between the genetic integration of virusbacteria and the expansion of some microbial population during tumorigenesis of human colorectum. Using a gut metagenomics sequencing data of healthy controls, advanced adenoma and carcinoma patients, to our knowledge, we demonstrate for the first time that the viral genetic integrations in gut microbes tend to occur in CRC patients and are potentially associated with the carcinogenesis. We found that almost all of the genetic integrations were happened between bacteriophages and bacteria, which could be influenced by the abundance of the phage communities. Importantly, the integrations of phage-carried positive effective genes offered selective advantages to the commensal and potential pathogenic bacteria, as a result, potentially led to a microbial dysbiosis along with the increasing bacterial diversity in carcinoma patients. Consequently, our work opens a new way to understand the carcinogenicity in complex intestinal ecosystems.

Evolutionary genetic integration of behavioural and endocrine components of the stress response

The vertebrate stress response comprises a suite of behavioural and physiological traits that must be functionally integrated to ensure organisms cope adaptively with acute stressors. The expectation that natural selection has favoured functional integration leads to a prediction of genetic integration: genetic variation in the stress response should include covariation between its component behavioural and physiological traits. Despite the implications of such genetic integration for our understanding of human and animal health, as well as evolutionary responses to natural and anthropogenic stressors, formal quantitative genetic tests of this prediction are lacking. Here we demonstrate that Trinidadian guppies (Poecilia reticulata) show genetic variation in a suite of behavioural and physiological components of the acute stress response, and that these are indeed integrated into a single major axis of genetic variation. This axis appears to reflect continuous variation in the magnitude of integrated stress responsiveness, rather than variation in ‘coping style’ (a verbal model that postulates equal levels of stress responsiveness will manifest differently across individuals). The genetic integration we find here could either facilitate or constrain evolutionary responses to selection, depending upon the extent to which the direction of selection aligns with this single major axis of genetic covariation among stress response traits. Such integration also suggests that, while stress-related disease typically arises from physiological components of the stress response, selection on the genetically correlated behavioural responses to stress could offer a viable non-invasive route to the genetic improvement of health and welfare in captive animal populations.