Host and Environmental Specificity in Bacterial Communities Associated to Two Highly Invasive Marine Species (Genus Asparagopsis)

Abstract

As habitats change due to global and local pressures, population resilience, and adaptive processes depend not only on their gene pools but also on their associated bacteria communities. The hologenome can play a determinant role in adaptive evolution of higher organisms that rely on their bacterial associates for vital processes. In this study, we focus on the associated bacteria of the two most invasive seaweeds in southwest Iberia (coastal mainland) and nearby offshore Atlantic islands, Asparagopsis taxiformis and Asparagopsis armata. Bacterial communities were characterized using 16S rRNA barcoding through 454 next generation sequencing and exploratory shotgun metagenomics to provide functional insights and a backbone for future functional studies. The bacterial community composition was clearly different between the two species A. taxiformis and A. armata and between continental and island habitats. The latter was mainly due to higher abundances of Acidimicrobiales, Sphingomonadales, Xanthomonadales, Myxococcales, and Alteromonadales on the continent. Metabolic assignments for these groups contained a higher number of reads in functions related to oxidative stress and resistance to toxic compounds, more precisely heavy metals. These results are in agreement with their usual association with hydrocarbon degradation and heavy-metals detoxification. In contrast, A. taxiformis from islands contained more bacteria related to oligotrophic environments which might putatively play a role in mineralization of dissolved organic matter. The higher number of functional assignments found in the metagenomes of A. taxiformis collected from Cape Verde Islands suggest a higher contribution of bacteria to compensate nutrient limitation in oligotrophic environments. Our results show that Asparagopsis-associated bacterial communities have host-specificity and are modulated by environmental conditions. Whether this environmental effect reflects the host's selective requirements or the locally available bacteria remains to be addressed. However, the known functional capacities of these bacterial communities indicate their potential for eco-physiological functions that could be valuable for the host fitness.

Keywords: Asparagopsis sp.; adaptation; bacterial communities; coastal vs. off-shore areas; eco-physiological functioning bacteria; metagenomes; polluted vs. pristine environments.

Figure 1

Sampling locations of Asparagopsis taxiformis (in pink) and Asparagopsis armata (in red). Asparagopsis taxiformis was sampled in Ilhéu da Forja (Madeira Island), Sines and Lagosteiros (Mainland Portugal) and in Tarrafal Beach (Cape Verde). Asparagopsis armata was sampled in three mainland locations: Lagosteiros, Praia do Queimado, and Zambujeira do Mar.

Figure 2

Rank abundance curves for each Asparagopsis group plotting logarithmic relative abundances.

Figure 3

Canonical analysis of Principle coordinates (CAP) plot showing the bacterial communities compositions of the main Asparagopsis groups (delimited according to previous statistical analyses). OTUs with Pearson's correlation >0.70 have been overlaid on the plot as vectors. Graphic was changed as described in the main text.

Figure 4

Differential clustering of the most abundant metabolisms of A. armata (mainland) and A. taxiformis (mainland and island). Normalized (following MG-RAST normalization procedure) values were used to draw the heatmap. The hierarchical dendrogram was clustered using Ward's minimum variance method with Bray-Curtis distance metric. Level 2 metabolisms of the most abundant level 1 metabolic assignments for Mainland samples (compared to island samples) were represented in pie charts and level 3, of the most relevant metabolism from level 2, was described. Absolute numbers of hits for the most representative functions are represented in the corresponding slice. AaML- A. armata mainland, AtML- A. taxiformis mainland, AtIsl- A. taxiformis Cape Verde. Graphics were manipulated to fit in the same figure (heatmap+pie charts) and pie charts colors were changed so the same feature color would match for all the samples (Raw data in Table S5).

Figure 5

Percentage of metagenomic sequences of functional composition of Level 2—Resistance to antibiotic and toxic compounds (assigned to the general SEED subsystems)—of Asparagopsis sps. from Mainland and Island (Raw data in Table S6).