Invasions and symbioses: multidimensional variability of the microbiome of an introduced ascidian species

Abstract

Abstract Background Animals should be viewed as holobionts, complex entities composed of an animal host and their associated symbionts. This integrated perspective recognizes that the interaction between these two components is vital for the survival of the host. This synergy can be particularly relevant in the case of invasive species, as they constantly face habitat changes, and thus play a crucial role in their introduction and adaptation success. However, our understanding on the microbiome changes of invasive species from juveniles to adults associated with different tissues remains limited.Results We reveal that the introduced ascidian Styela plicata has a highly variable microbiome, which undergoes significant changes from juvenile to adult individuals and is highly specialised for each compartment analysed (tunic, gill, and gut) in different localities. This is the first time that a distinct gill microbiome is identified in an ascidian species. The variability observed is attributed to S. plicata’s ability to acquire its resident bacteria from the surrounding water, with a subsequent differential proliferation leading to the development of clearly differentiated microbiomes in each tissue. We also observe that the microbiome varies across harbours, suggesting adaptation to local environmental conditions. Furthermore, we find that each tissue’s microbiome is strongly correlated with environmental trace element concentrations, especially in adults, where trace element levels are higher. This fact suggests that the microbiome of S. plicata can play a role by either taking advantage or disposing of trace elements, many of which are toxic. Finally, we examine the metabolic pathways attributable to each microbiome, revealing that adult microbiomes have specific metabolic pathways that might enhance tissue functionality, conferring a high adaptive potential to S. plicata to withstand new conditions during the introduction process, turning this species into one of the most successful invasive holobionts worldwide.Conclusions Our findings emphasise the need for integrative approaches to investigate animal microbiomes, considering multiple variables to fully comprehend the relationship between host and microbiome, as well as their implications for host integrity. Thus, this work confirms the complex interplay between S. plicata and its microbiomes, and how it has significant implications for the invasive success of this species.