Entangled fates of holobiont genomes during invasion: nested bacterial and host diversities in Caulerpa taxifolia

Abstract

Successful prevention and mitigation of biological invasions requires retracing the initial steps of introduction, as well as understanding key elements enhancing the adaptability of invasive species. We studied the genetic diversity of the green alga Caulerpa taxifolia and its associated bacterial communities in several areas around the world. The striking congruence of α and β diversity of the algal genome and endophytic communities reveals a tight association, supporting the holobiont concept as best describing the unit of spreading and invasion. Both genomic compartments support the hypotheses of a unique accidental introduction in the Mediterranean and of multiple invasion events in southern Australia. In addition to helping with tracing the origin of invasion, bacterial communities exhibit metabolic functions that can potentially enhance adaptability and competitiveness of the consortium they form with their host. We thus hypothesize that low genetic diversities of both host and symbiont communities may contribute to the recent regression in the Mediterranean, in contrast with the persistence of highly diverse assemblages in southern Australia. This study supports the importance of scaling up from the host to the holobiont for a comprehensive understanding of invasions.

The Microbiome of the Worldwide Invasive Ascidian Didemnum vexillum

“…For introduced marine species in general, it has been pointed out that the microbial symbiont community can contribute to the survival and adaptation of the holobiont during the invasion process. Several mechanisms have been proposed, such as heavy metal detoxification (Aires et al, 2016), production of toxic chemicals that can increase competitive ability on a new habitat (Amsellem et al, 2017), or enhanced nutrient fixation (Arnaud-Haond et al, 2017). Likewise, broadly introduced species face diverse temperature regimes, and microbial symbionts have been shown to play a role in adaptation of invertebrates to temperature changes (e.g., in corals: Ziegler et al, 2017;Osman et al, 2020).…”

Climate Change Impacts on Seagrass Meadows and Macroalgal Forests: An Integrative Perspective on Acclimation and Adaptation Potential

“…Holobiont evolution requires strict partner fidelity and will only work under vertical transmission fidelity and can be evolutionary unstable due to microbial cheaters, or shifting cost:benefit ratios (Douglas and Werren, 2016). However, the persistence of co-introduced symbiont bacteria many decades after macroalgae invaded in the Mediterranean from Australia, and their correlation with the host ecology (Aires et al, 2013;Arnaud-Haond et al, 2017), suggests a tight inter-dependence in at least some invasive macroalgae lineages. Notwithstanding, positive functional roles of the host-associated microbiome are also possible if the microbiome and its host do not evolve as a strict unit.…”

Propagule composition regulates the success of an invasive seaweed across a heterogeneous seascape

“…Positive effects of −F+R on +F+R could be explained by below‐ground processes, which have so far received little regard in the success of marine macrophytes in marine sediment systems, despite them being some of the most invasive species in the world (but see Gribben et al, ; Gribben et al, ). In Caulerpales, rhizoids are root‐like structures associated with specific bacteria that enhance carbon, nitrogen (including amino acids) and phosphorous uptake from the substratum (Arnaud‐Haond et al, ; Chisholm, Dauga, Ageron, Grimont, & Jaubert, ; Rizzo et al, ). Thus, 22‐cm long −F+R fragments, by virtue of their high number of rhizoid clusters, may have enhanced the success of +F+R fragments allowing a more rapid conditioning of the sediment microbiota without, at least in the first stages of establishment, reducing light levels.…”