The Microbiome of the Worldwide Invasive Ascidian Didemnum vexillum

Abstract

All multicellular organisms, including ascidians, host diverse microbial communities that are essential for their evolution. The global invader Didemnum vexillum is a colonial species native to Japan with two main genetic clades, A (the only invasive) and B, which provides a unique opportunity to assess if the microbiome remains stable in the colonization process or shifts according to local environment. We have analyzed, using 16S amplicon sequencing, the microbiome of 65 D. vexillum colonies from 13 populations worldwide including the two clades in the native area, plus samples from a congeneric species and seawater from one of the localities. We found 3,525 zeroradius operational taxonomic units (ZOTUs) in D. vexillum, belonging to 36 bacterial and 3 archaeal phyla. The microbiome of this species had a markedly different composition from surrounding seawater and from the congeneric species. For the globally invasive clade A, we found 3,154 ZOTUs, and 8 of them were present in all colonies, constituting a core microbiome with high abundance (69.57% of the total reads) but low diversity (0.25% of the total number of ZOTUs). The variable component was quantitatively much less important but comprised a highly diverse assemblage. In a multiple regression model, global microbiome structure correlated with differences in temperature range across localities and also with geographic distances, pointing to horizontal acquisition of the symbionts. However, the ascidian may have a strong capacity to select and enrich its microbiome, as we found that the most abundant ZOTUs from tunic samples had low abundance in seawater samples from the same locality. The microbiome structure also correlated with the genetic distances between colonies obtained in a previous genomewide analysis, suggesting some potential for vertical transmission. In geographically restricted comparisons, temperature and genetic makeup, but not geography, explained microbiome structure. The combination of a quantitatively dominant core component and a highly diverse variable fraction in the microbiome of D. vexillum can contribute to the success of this global invader in different environments.

Looks can be deceiving: Didemnum pseudovexillum sp. nov. (Ascidiacea) in European harbours

“…The number of coils in the sperm duct is also lower (6-7) than in Didemnum vexillum (8-11, Lambert 2009;Ordóñez et al 2015). Finally, a recent study (Casso et al 2020) showed that the microbiome communities of Didemnum vexillum and Didemnum pseudovexillum sp. nov. (referred to as Didemnum sp.…”

“…in that work) were also markedly different. In Casso et al (2020), the microbiome of Didemnum vexillum in its native and introduced range was examined, and samples of Didemnum pseudovexillum were used for comparison, showing that even congeneric species living in the same kind of environment had species-specific microbiomes.…”

Comparative Microbiome and Metabolome Analyses of the Marine Tunicate Ciona intestinalis from Native and Invaded Habitats

“…Previous studies suggested that both symbiont recruitment strategies, vertical and horizontal transmission, play crucial, complementary roles for survival, but also establishment of invasive ascidians in new ecosystems [ 25 , 60 , 61 , 73 ]. Vertical symbiont transmission (intergenerational transfer of core microbes) ensures stability of core microbiota and their functions in host health, but is considered to lower the adaptability of the macrobiont [ 25 , 61 ].…”

Cryptic genetic lineages of a colonial ascidian host distinct microbiomes

“…These microbial communities inhabit both the tunic and the zooids of the animal (Blasiak et al., 2014; Erwin et al., 2014; Schreiber, Kjeldsen, Funch, et al., 2016), and despite the fact that sea squirts are filter feeders, remain structurally and compositionally distinct from the bacterioplankton community of the surrounding water (Dror et al., 2019; Erwin et al., 2014; Evans et al., 2017). Some of these symbionts appear to be horizontally sourced from the seawater microbial seed bank, and their numbers then amplified within optimal ‘microniches’ in the ascidian tunic (Behrendt et al., 2012; Casso et al., 2020; Erwin et al., 2014). Interestingly, ascidian microbial communities are also highly host‐specific (Erwin et al., 2014; Evans et al., 2017; Tianero et al., 2015), with significant differences detectable even among congeneric and closely related species (Evans et al., 2017) and between native and introduced populations of invasive species (Casso et al., 2020; Goddard‐Dwyer et al.…”

“…Some of these symbionts appear to be horizontally sourced from the seawater microbial seed bank, and their numbers then amplified within optimal ‘microniches’ in the ascidian tunic (Behrendt et al., 2012; Casso et al., 2020; Erwin et al., 2014). Interestingly, ascidian microbial communities are also highly host‐specific (Erwin et al., 2014; Evans et al., 2017; Tianero et al., 2015), with significant differences detectable even among congeneric and closely related species (Evans et al., 2017) and between native and introduced populations of invasive species (Casso et al., 2020; Goddard‐Dwyer et al. 2021).…”