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Chemical and pathogenic hazards in aquaculture supply chains threaten the provision of safe aquatic food. The Seafood Risk Tool is an integrated, semi-quantitative system that develops bespoke supply chain and risk management strategies.Although wild fish catches have plateaued globally, the aquaculture sector continues to expand in response to increasing demand for fish and other aquatic foods. Economic progress and the growing consumer awareness of aquatic foods in sustainable, healthy and nutritious diets are contributing to sector expansion1. However, rapid expansion must be achieved in a socially responsible and environmentally sustainable manner. Aquaculture produces over 400 different species across marine and freshwater fish, crustaceans, molluscs, plants and algae2 — all presenting complex and unique risk profiles to the environment, the industry, investors and consumers. Measures to mitigate these risks, including aquaculture certification and legislation, are inconsistent across nations and regions, and cohesive risk management has been difficult to manage and implement. More

Barcoding of Pseudomonas isolates and experimental designTo test possible host–commensal–pathogen dynamics in a local population, we spray inoculated six A. thaliana accessions with synthetic bacterial communities composed of pathogenic and commensal Pseudomonas candidates. Because we wanted to study interactions that are likely to occur in nature, we used A. thaliana genotypes that originated from the same plant populations near Tübingen, Germany28, from which the Pseudomonas strains had been isolated (Fig. 1a). Classification of Pseudomonas lineages as pathogenic or commensal was based on observed effects in axenic infections11. Only one lineage, previously named OTU5, which dominated local plant populations, was associated with pathogenicity, both based on negative impact on rosette weight and visible disease symptoms11. We henceforth call this lineage ATUE5 (isolates sampled from ‘Around TUEbingen, group 5’) and all other Pseudomonas lineages from the Karasov collection non-ATUE5. We interchangeably use the terms ‘pathogens’ or ‘ATUE5’, and ‘commensals’ or ‘non-ATUE5’.Fig. 1: Study system.a, Location of original a. thaliana and Pseudomonas sampling sites around Tübingen. b, Taxonomic representation of the 14 Pseudomonas isolates used and the prevalence of closely related strains (divergence 0.99 and P value |± 0.2| shown. Node colours indicate the bacterial isolate classification, ATUE5 or non-ATUE5. e, In planta abundance change of the seven ATUE5 isolates in non-ATUE5 inclusive treatments in comparison with PathoCom. Abundance mean difference was estimated with the model [log10(isolate load) ~ treatment × experiment + treatment + experiment + error] for each individual strain. Thus, the treatment coefficient was estimated per isolate. Dots indicate the median estimates, and vertical lines represent 95% Bayesian credible intervals of the fitted parameter. ‘Combi’ indicates combination of the isolates C3,C4,C5 and C7, and n = 23.Full size imageEach of the 14 isolates was examined for growth inhibition against all other isolates, covering all possible combinations of binary interactions. In total, three strains out of the 14 had inhibitory activity; all were non-ATUE5 (Fig. 4c). Specifically, C4 and C5 showed the same pattern: both inhibited all pathogenic isolates but P1, and both inhibited the same two commensals, C6 and weakly C3. C3 inhibited three ATUE5 isolates: P5, P6 and P7. In summary, the in vitro assay provides evidence that among the tested Pseudomonas isolates, direct inhibition was a trait unique to commensals, and susceptible bacteria were primarily pathogens. This supports the notion that ATUE5 and non-ATUE5 isolates employ divergent competition strategies, or that if they use the same mechanism, they differ in the effectiveness of such a mechanism.The in vitro results recapitulated the general trend of pathogen inhibition found among treatments in planta. Nevertheless, we observed major discrepancies between the two assays. First, P1 was not inhibited by any isolate in the host-free assay (Fig. 4c), though it was the most inhibited member in planta among the communities (Fig. 4b). Second, no commensal isolate was inhibited in planta among communities (Fig. 4b), while two commensals, C3 and C6, were inhibited in vitro (Fig. 4c). Both observations are compatible with an effect of the host on microbe–microbe interactions. To explore such effects, we analysed all pairwise microbe–microbe abundance correlations within MixedCom-infected hosts. When we used absolute abundances, all pairwise correlations were positive, also in CommenCom and PathoCom (Extended Data Fig. 8a), consistent with there being a positive correlation between absolute abundance of individual isolates and total abundance of the entire community (Supplementary Fig. 7), that is, no isolate was less abundant in highly colonized plants than in sparsely colonized plants. This indicates that there does not seem to be active killing of competitors in planta in the CommenCom, which is probably not surprising. With relative abundances, however, a clear pattern emerged with a cluster of commensals that were positively correlated, possibly reflecting mutual growth promotion, and several commensal strains being negatively correlated with both P6 and C7, possibly reflecting unidirectional growth inhibition (Fig. 4d). We did not observe the same correlations within CommenCom among commensals and within PathoCom among pathogens as we did for either subgroup in MixedCom, reflecting higher-order interactions. Thus, interactions among pathogens were constrained by the presence of commensals and vice versa (Extended Data Fig. 8b).The in planta patterns measured in complex communities did not fully recapitulate what we had observed in vitro with pairwise interactions. We therefore investigated individual commensal isolates for their ability to suppress pathogens in planta and also tested the entourage effect. We focused on the three commensals C3, C4 and C5, which had directly inhibited pathogens in vitro, and as a control C7, which had not shown any inhibition activity in vitro. We infected plants with mixtures of PathoCom and each of the four individual commensals and also with PathoCom mixed with all four commensals. Because pathogen inhibition seemed to be independent of the host genotype, we arbitrarily chose HE-1. Regardless of the commensal isolate, only P1 was suppressed with high probability in all commensal-including treatments (Fig. 4e), with P2, P3 and P4 being substantially inhibited only by the mixture of all four commensals. Together with the lack of meaningful differences between individual commensals, this indicates that pathogen inhibition is either a function of commensal dose or a result of interaction among commensals.An important finding was that four commensal strains had much more similar inhibitory activity in planta than in vitro and that the combined action was greater than the individual effects. Together, this suggested that the host contributes to the observed interactions between commensal and pathogenic Pseudomonas isolates. To begin to investigate this possibility, we next studied potential host immune responses with RNA sequencing.Defensive response elicited by non-ATUE5For the RNA-sequencing experiment, we treated plants of the genotype Lu3-30 with the three synthetic communities and also used a bacteria-free control treatment. We sampled the treated plants 3 DPI and 4 DPI, thus increasing the ability to pinpoint differentially expressed genes (DEGs) between treatments that are not highly time specific. Exploratory analysis indicated that the two time points behaved similarly, and they were combined for further in-depth analysis.We first looked at DEGs in a comparison between infected plants and control (Supplementary Table 5); with PathoCom, there were only 14 DEGs; with CommenCom, there were 1,112 DEGs; and with MixedCom, there were 1,949 DEGs, suggesting that the CommenCom isolates, which are also present in the MixedCom, elicited a stronger host response than the PathoCom members. Furthermore, the high number of DEGs in MixedCom, higher than both PathoCom and CommenCom together, suggested a synergistic response derived from inclusion of both PathoCom and CommenCom members. Alternatively, this could also be a consequence of the higher initial inoculum in the 14-member MixedCom than either the 7-member PathoCom or 7-member CommenCom, or a combination of the two effects (Fig. 5a,b and Extended Data Fig. 9). The genes induced by the MixedCom fell into two classes: Group 5 (Fig. 5a,b) was also induced, albeit more weakly, by the CommenCom but not by the PathoCom. This group was overrepresented for non-redundant gene ontology (GO) categories linked to defence (Fig. 5c) and most likely explains the protective effects of commensals in the MixedCom. Specifically, among the top ten enriched GO categories in the shared MixedCom and CommenCom set, eight relate to immune response or response to another organism (‘defence response’, ‘multi-organism process’, ‘immune response’, ‘response to stimulus’, ‘response to biotic stimulus’, ‘response to other organism’, ‘immune system process’, ‘response to stress’; Fig. 5c).Fig. 5: Only commensal members elicit a strong host-defensive response.a, Relative expression (RE) pattern of 2,727 DEGs found in at least one of the comparisons of CommenCom, PathoCom and MixedCom with Control. DEGs were hierarchically clustered. b, Euler diagram of DEGs in PathoCom-, CommenCom- and MixedCom-treated plants compared with Control (log2[fold change]  >|± 1|; false discovery rate (FDR) 0.05); n = 4.Full size imageGroup 4 was only induced in MixedCom, either indicating synergism between commensals and pathogens or reflecting a consequence of the higher initial inoculum. This group included a small number of redundant GO categories indicative of defence, such as ‘salicylic acid mediated signalling pathway’, ‘multi-organism process’, ‘response to other organism’ and ‘response to biotic stimulus’ (Supplementary Table 6). Moreover, the MixedCom response cannot simply be explained by synergistic effects or commensals suppressing pathogen effects because there was a prominent class, Group 2, which included genes that were induced in the CommenCom but to a much lesser extent in the PathoCom or MixedCom. From their annotation, it was unclear how they can be linked to infection (Fig. 5c). About 500 genes (Group 1) that were downregulated by all bacterial communities are unlikely to contain candidates for commensal protection (Fig. 5a).Cumulatively, these results imply that the CommenCom members elicited a defensive response in the host regardless of PathoCom members, while the mixture of both led to additional responses. To better understand if selective suppression of ATUE5 in MixedCom infections may have resulted from the recognition of both non-ATUE5 and ATUE5 (reflected by a unique MixedCom set of DEGs) or solely non-ATUE5 (a set of DEGs shared by MixedCom and CommenCom), we examined the expression of key genes related to the salicylic acid pathway and downstream immune responses. Activation of the salicylic acid pathway was previously related to increased fitness of A. thaliana in the presence of wild bacterial pathogens, a phenomenon which was attributed to an increased systemic acquired resistance32.We observed a general trend of higher expression in MixedCom- and CommenCom-infected hosts for several such genes (Fig. 5d). Examples are PR1 and PR5, marker genes for systemic acquired resistance and resistance execution. Therefore, according to the marker genes we tested, non-ATUE5 elicited a defensive response in the host, regardless of ATUE5 presence.We conclude that the expression profiles of non-ATUE5-infected Lu3-30 plants point to an increased defensive status, supporting our hypothesis regarding host-mediated ATUE5 suppression. We note that ATUE5 suppression was not associated with full plant protection and thus control-like weight levels in all plant genotypes. One accession, Ey15-2, was only partially protected in the MixedCom (Fig. 2), despite levels of pathogen inhibition being not very different from other host genotypes (Extended Data Fig. 7).Lack of protection explained by a single pathogenic isolateThe fact that Ey15-2 was only partially protected by MixedCom (Fig. 2) underlines the importance of the host genotype in plant–microbe–microbe interactions, apparently reflecting the dynamics between microbes and plants in wild populations. We therefore wanted to reveal the cause for this differential interaction.Our first aim was to rank compositional variables in MixedCom according to their impact on plant weight, regardless of host genotype. Next, we asked whether any of the top-ranked variables could explain the lack of protection in Ey15-2. With Random Forest analysis, we estimated the weight-predictive power of all individual isolates in MixedCom and three cumulative variables: total bacterial abundance, total ATUE5 abundance and total non-ATUE5 abundance. We found that the best weight-predictive variable was the abundance of pathogenic isolate P6, followed by total bacterial load and total ATUE5 load, which were probably confounded by the abundance of P6 (Fig. 6a). In agreement, P6 was the dominant ATUE5 in MixedCom (Fig. 6b and Extended Data Fig. 10a). We thus hypothesized that the residual pathogenicity in MixedCom-infected Ey15-2 was caused by P6. Although P6 grew best in Ey15-2, the difference to most other genotypes was unlikely to be important (Extended Data Fig. 10b). However, P6 was particularly dominant in Ey15-2 (Fig. 6b).Fig. 6: The effect of isolate P6 on weight in MixedCom-infected hosts and particularly on accession Ey15-2.a, Relative importance (mean decrease accuracy; ‘MSE’) of 20 examined variables in weight prediction of MixedCom-infected hosts as determined by Random Forest analysis. The best predictor was the abundance of isolate P6. ‘Total bacterial’, ‘Total ATUE5’ and ‘Total non-ATUE5’ indicate the cumulative abundances of the 14 isolates, seven ATUE5 isolates and seven non-ATUE5 isolates, respectively. b, Abundance of P6 compared with the other 13 barcoded isolates in MixedCom-infected hosts across the six A. thaliana genotypes used in this study. Dots indicate the median estimates, and vertical lines represent 95% Bayesian credible intervals of the fitted parameter, following the model [log10(isolate load) ~ isolate × experiment + isolate + experiment + error]. Each genotype was analysed individually, thus the model was utilized for each genotype separately. The shaded area denotes the 95% Bayesian credible intervals for the isolate P6. c, Fresh rosette weight of Ey15-2 plants treated with Control, MixedCom and MixedCom without P6 (MixedCom ΔP6). Fresh rosette weight was measured 12 DPI. The top panel presents the raw data, with the breaks in the vertical black lines denoting the mean value of each group, and the vertical lines indicating standard deviation. The lower panel presents the mean difference to control, plotted as bootstrap sampling55,56, indicating the distribution of effect size that is compatible with the data. The 95% confidence intervals are indicated by the black vertical bars, and n = 19.Full size imageGiven that pathogen load in Ey15-2 was driven to a substantial extent by P6, we assumed that this isolate had a stronger impact on the weight of Ey15-2 than on other accessions. We experimentally validated that removal of P6 restored protection when Ey15-2 was infected with the MixedCom (Fig. 6c). To confirm that restored protection was due to the interaction of commensals with the five other pathogenic isolates (P1–P5), rather than simply removal of P6, we also treated Ey15-2 with PathoCom only, but not P6. The removal of P6 did not diminish the negative weight impact of PathoCom (P1–P5, Supplementary Fig. 8), implying that it was indeed the interaction between commensals with five out of six pathogenic isolates that mitigated the harmful effect of pathogens in Ey15-2 plants. More

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