Simulating a biological invasion in the lab: picky seaweeds are poor invaders

Seaweeds are a major group of invasive species. As holobionts they are colonized by microbial symbionts. The conditions during cross-oceanic transport are often extreme. How does an invasive seaweed deal with holobiont disturbance? How are its microbial communities reassembled in a new environment?
Published in Microbiology
Simulating a biological invasion in the lab: picky seaweeds are poor invaders

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Figure 1. The invasive red seaweed Agarophyton vermiculo-
. Photo by Stacy Krueger-Hadfield. 

Like plants in terrestrial ecosystems, seaweeds fulfill important roles in coastal marine habitats. They are actually a polyphyletic group composed of three diverse evolutionary lineages. Red and green seaweeds are in the same overall lineage as angiosperms, whereas brown seaweeds are in an entirely different group including oomycetes and diatoms. Similar to plants, seaweeds are holobionts and interact intimately with microbial symbionts.

Human activities have both intentionally and unintentionally distributed organisms, including seaweeds, across the planet for hundreds if not thousands of years, resulting in substantial numbers of biological invasions. However, the conditions during transport from one region to another are often extreme, including for example drought, darkness and anoxia for long time periods. Most seaweeds cannot survive this and only a small proportion becomes invasive. These harsh conditions do not simply affect the seaweed, but they also radically disturb the microbial communities in the holobiont, likely killing most symbionts. How do invasive seaweeds deal with disturbed microbial communities. Are they able to assemble new functional communities in a different environment? And does a capacity to reassemble communities promote invasiveness?

To address these questions we conducted an experiment of which the results have now been published in the ISME Journal. As it is impossible to sample a seaweed before and after it has been introduced to a new environment and has successfully established, addressing these questions was a challenging adventure.

The invasive seaweed holobiont
Joining forces with colleagues from China, Japan, and the USA, we designed an experiment to 'simulate' an invasion using the widespread invader Agarophyton vermiculophyllum as a model invasive holobiont (Figure 1). This red seaweed has spread from north-east Asia to Europe and the west and east coasts of North America. As we learned from earlier work with the same international team, its microbiota differ between the native and non-native range, but also share a geography independent 'core' of microbes.

Simulating an invasion
We sampled and collected the seaweed from sites in California, Virginia, France, Germany, China, and Japan during a two-week period (many kilometers of driving to remote locations and processing samples until very late at night). The seaweed samples were transported to Kiel (Germany) where a new artificial environment was created under controlled conditions in our lab. To mimic severe holobiont disturbance during cross-oceanic transport, we exposed the seaweeds to a cocktail of antibiotics and then to a mixture of microbes, created from extracts of all the sites we sampled to represent a new source of microbes to which an invader has access upon introduction. To record how the microbial communities in the holobionts changed right after disturbance, but also over a longer stretch of time, we sampled each seaweed repeatedly to extract DNA and characterize the microbial communities based on 16S rDNA amplicon sequencing.

Inside the invasive holobiont
Hundreds of DNA extractions, PCRs, and months of data processing and analysis later, we could finally have a look into the invasive holobiont.

  • New microbial communities. Microbial communities of treated seaweeds completely changed, both in terms of composition and function. While compositionally the communities remained different (Figure 2A) from those observed in the control group, after six weeks they did become similar in most functional respects.
  • Invaders are more flexible. Interestingly, microbial communities of non-native populations (Europe and North America) became more similar to one another than those from the native populations (Asia, Figure 2B). In turn, microbial communities associated with those from the native range remained more similar to the composition observed in the field (Figure 2C). In other words, the native seaweeds seemed pickier toward microbial symbionts and less flexible than the non-natives.
  • Invaders perform better. Finally, more flexible non-native seaweeds performed better in the artificial environment, suggesting these flexible holobionts are more invasive.

Altogether, our simulated invasion demonstrates how a seaweed host that is more flexible towards symbionts may be more invasive. It also provides evidence that the invasion process itself may select for more flexible hosts. For more details, check out the paper!

Figure 2. Compiled from Bonthond et al. (2021). A An nMDS plot, visualizing the similarity between microbial communities in a two dimensional space (the larger the distance, the more dissimilar). Succession trajectories of microbial communities living on disturbed seaweeds (red arrow) differ from the control group (blue arrow). B Dissimilarity (measured in Bray-Curtis distance) displayed between microbial communities after disturbance displayed over time. Microbial communities from native holobionts (grey) are more dissimilar than non-native holobionts (red). C Dissimilarity between microbial communities after disturbance and in the field. Communities from non-native holobionts (red) are more dissimilar from the field than native holobionts (grey).

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