Integration of spatio-temporal variations of surface metabolomes and epibacterial communities highlights the importance of copper stress as a major factor shaping host-microbiota interactions within a Mediterranean seaweed holobiont

Abstract

Background Although considered as holobionts, macroalgae and their surface microbiota share intimate interactions that are still poorly understood. Little is known on the effect of environmental parameters on the close relationships between the host and its surface-associated microbiota, and even more in a context of coastal pollutions. Therefore, the main objective of this study was to decipher the impact of local environmental parameters, especially trace metal concentrations, on an algal holobiont dynamics using the Phaeophyta Taonia atomaria as a model. Through a multidisciplinary multi-omics approach combining metabarcoding and untargeted LC-MS-based metabolomics, the epibacterial communities and the surface metabolome of T. atomaria were monitored along a spatio-temporal gradient in the bay of Toulon (Northwestern Mediterranean coast) and its surrounding. Indeed, this geographical area displays a well-described trace metal gradient particularly relevant to investigate the effect of such pollutants on marine organisms. Results Epibacterial communities of T. atomaria exhibited a high specificity whatever the five environmentally contrasted collecting sites investigated on the NW Mediterranean coast. By integrating metabarcoding and metabolomics analyses, the holobiont dynamics varied as a whole. During the occurrence period of T. atomaria, epibacterial densities and α-diversity increased while the relative proportion of core communities decreased. Pioneer bacterial colonizers constituted a large part of the specific and core taxa, and their decrease might be linked to biofilm maturation through time. Then, the temporal increase of the Roseobacter was proposed to result from the higher temperature conditions, but also the increased production of dimethylsulfoniopropionate (DMSP) at the algal surface which could constitute of the source of carbon and sulfur for the catabolism pathways of these taxa. Finally, as a major result of this study, copper concentration constituted a key factor shaping the holobiont system. Thus, the higher expression of carotenoids suggested an oxidative stress which might result from an adaptation of the algal surface metabolome to high copper levels. In turn, this change in the surface metabolome composition could result in the selection of particular epibacterial taxa. Conclusion We showed that associated epibacterial communities were highly specific to the algal host and that the holobiont dynamics varied as a whole. While temperature increase was confirmed to be one of the main parameters associated to Taonia dynamics, the originality of this study was highlighting copper-stress as a major driver of seaweed-epibacterial interactions. In a context of global change, this study brought new insights on the dynamics of a Mediterranean algal holobiont submitted to heavy anthropic pressures.

Synergistic effects of temperature and light affect the relationship between Taonia atomaria and its epibacterial community: a controlled conditions study

“…In a general context of global change, the impact of environmental factors on the surface microbiota of marine holobionts is still poorly studied through controlled conditions experiments and the combination with the surface host's metabolome characterization remains rare. In the case of T. atomaria, the concurrent temporal increase of temperature and irradiance has been hypothesized to play a key role in controlling seaweed-microbiota interactions in natural environment (Paix et al, 2019;Paix et al, 2020b), while a decrease of these parameters had been never investigated before. The aim of this study was to decouple these two factors to understand their specific and synergistic effects on the host-surface microbiota interactions.…”

“…The global annotation was performed as described in Paix et al (2019Paix et al ( , 2020a and Carriot et al (2021). Briefly, the annotation was based on the use of an 'in-house' database described in Carriot et al (2021), gathering metabolites annotated through the use of molecular networks (details in SI).…”

“…The objective of this 'controlled conditions experiment' was to decipher the respective and synergistic effects of temperature and irradiance on the interactions between T. atomaria and its epibacterial community. The temperature values were chosen according to the natural in situ variations observed during the summer, when the epibiotic community is stabilized (Paix et al, 2019). As temperatures follow an increase and then a decrease from the beginning to the end of the summer along coasts of north Brittany, three different temperatures were chosen: an ambient one corresponding to the field measures in June (18 C named AT for ambient temperature), together with higher and lower ones corresponding to the extremes observed within this period (13 C and 22 C named LT and HT respectively for low and high temperatures).…”

“…Such metabolites have been hypothesized to be part of the algal chemical defences and involved in the selection of a specific epibacterial community. Furthermore, strong seasonal correlations occur, notably during spring and summer, between specific surface metabolites and some epibacterial taxa (Paix et al ., 2019). In the light of these results and those previously obtained for the algal model F .…”

“…atomaria , the field studies have not delineated the respective effects of colinear factors such as temperature and light. Due to their temporal covariations, their relative importance is now questioned according to the important seasonal effect observed as part of in situ studies (Paix et al ., 2019, submitted ).…”