Metabolic constraints for a novel symbiosis

Abstract

Ancient evolutionary events are difficult to study because their current products are derived forms altered by millions of years of adaptation. The primary endosymbiotic event formed the first photosynthetic eukaryote resulting in both plants and algae, with vast consequences for life on Earth. The evolutionary time that passed since this event means the dominant mechanisms and changes that were required are obscured. Synthetic symbioses such as the novel interaction between Paramecium bursaria and the cyanobacterium Synechocystis PC6803, recently established in the laboratory, permit a unique window on the possible early trajectories of this critical evolutionary event. Here, we apply metabolic modelling, using flux balance analysis (FBA), to predict the metabolic adaptations necessary for this previously free-living symbiont to transition to the endosymbiotic niche. By enforcing reciprocal nutrient trading, we are able to predict the most efficient exchange nutrients for both host and symbiont. During the transition from free-living to obligate symbiosis, it is likely that the trading parameters will change over time, which leads in our model to discontinuous changes in the preferred exchange nutrients. Our results show the applicability of FBA modelling to ancient evolutionary transitions driven by metabolic exchanges, and predict how newly established endosymbioses, governed by conflict, will differ from a well-developed one that has reached a mutual-benefit state.

Mechanisms and Impact of Symbiotic Phosphate Acquisition

“…Evolutionarily younger, artificial symbioses similarly reveal the gradual evolution of auxotrophy and nutritional interdependence for mutualism to develop. This includes the Chlamydomonas reinhardtii-Saccharomyces cerevisiae exchange of carbon and nitrogen (Hom and Murray 2014); Lobomonas rostrate-Mesorhizobium loti exchange of carbon for Vitamin B12 (Helliwell et al 2018); as well as Synechocystis PCC6803-Paramecium bursaria exchange of carbon for nitrogen (Sørensen et al 2016), to name a few.…”

Simulating the evolutionary trajectories of metabolic pathways for insect symbionts in the genus Sodalis

“…There are several published examples of using FBA to analyse the metabolism of symbiotic bacteria, including for Buchnera aphidicola [ 7, 30, 31 ], Sodalis glossinidius [ 32, 33 ], ' Candidatus Portiera aleyrodidarum' [ 34 ], Hamiltonella defensa [ 34 ] and strains of Blattabacterium [ 35 ]. There are also models published for the Synechocystis species used in the study of artificially induced symbiosis [ 36–40 ]. FBA is useful in this instance, as experiments that would not be possible empirically, due to culturability issues, can be performed in silico .…”

Simulating the evolutionary trajectories of metabolic pathways for insect symbionts in the Sodalis genus

“…There are several published examples of using FBA to analyse the metabolism of symbiotic bacteria, including for Buchnera aphidicola (Macdonald et al, 2012, 2011; Thomas et al, 2009), Sodalis glossinidius (Belda et al, 2012; Hall et al, 2019), Portiera aleyrodidarum (Ankrah et al, 2017), Hamiltonella defensa (Ankrah et al, 2017) and strains of Blattabacterium (González-Domenech et al, 2012). There are also models published for the Synechocystis species used in the study of artificially induced symbiosis (Knoop et al, 2013, 2010; Nogales et al, 2012; Shastri and Morgan, 2005; Sørensen et al, 2016). FBA is useful in this instance, as experiments that would not be possible empirically, due to culturability issues, can be performed in silico .…”