Replaying the tape of ecology to domesticate wild microbiota

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Abstract

Humanity has benefited from the domestication of nature and there is an increasing need to predict and control ecosystems. Domesticating bacterial communities would be particularly useful. Bacterial communities play key roles in global biogeochemical cycles, in industry (e.g. sewage treatment, fermented food and drink manufacturing), in agriculture (e.g. by fixing nitrogen and suppressing pathogens), and in human health and animal husbandry. There is therefore great interest in understanding bacterial community dynamics so that they can be controlled and engineered to optimise ecosystem services. We assessed the reproducibility and predictability of bacterial community dynamics by creating a frozen archive of hundreds of naturally-occuring bacterial communities that were repeatedly revived and tracked in a standardised, complex environment. Replicate communities followed reproducible trajectories and the community dynamics could be closely mapped to ecosystem functioning. However, even under standardised conditions, the communities exhibited tipping-points, where a small difference in initial community composition created divergent outcomes. We accurately predicted ecosystem outcomes based on initial bacterial community composition, and identified the conditions under which divergent ecosystem outcomes may be expected. In conclusion, we have shown the feasibility of our approach to reproducibly achieve predictable compositions and functions from wild communities. Nonetheless, the predictability of community trajectories, and therefore their utility in domestication, requires detailed knowledge of rugged compositional landscapes where ecosystem properties are not the inevitable result of prevailing environmental conditions but can be tilted toward different outcomes depending on the initial community composition.

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  1. Regardless of the underlying mechanism, both the metagenomic profiles and the functional experiments demonstrate that the the final community classes are not just alternative taxonomic variants providing the same functional outcome, but that the divergent community classes translate into significant functional differences. The two final classes are therefore unlikely to result from neutral community drift.

    This is a very elegant demonstration.

  2. Final Class 1 communities had higher degradation rates and enzymatic activity

    This is great to have measured the functional performance. Do we know how this compare to the 'natural' performance in the ponds?

  3. This analysis suggested that the 2 community classes were associated with distinct modes of nutrient uptake

    If the authors have any metagenomic information about the original or in situ sample (the one directly from the pound, that would be nice to compare with the domesticated community how this has changed.

  4. re-grown repeatedly

    Does this mean that 4 replicates have been grown for 7 days (without transfer) for each sample (and for a single round), or that each replicate has been grown for multiple consecutive rounds of 7 days to check stability of the community composition?

  5. co-occurring biota

    Is the microbial community of this environment uniquely bacteria? I wonder if other microorganisms such as fungi or protists are also parts of the microbial ecosystems and how much they interact with the bacterial community and the beech degradation function? What is the authors rational behind domesticating only bacteria?

  6. We quantified the taxonomic composition of the communities before they were revived

    Cryopreservation may have affected the community composition. Have the authors also looked at the community just after thawing the sample, to have an idea of the 'living' composition of the starting community? Would this be an important information to have to control or understand the process of reproducible domestication?

  7. We quantified the taxonomic composition of the communities before they were revived from cryopreservation (starting communities) and their composition and functioning at the end of the experiment (final communities), allowing us understand their reproducibility and trajectory and therefore their potential for domestication.

    Looking at Figure 1, it seems that the authors have taken samples that were initially grown for 7 days before cryopreservation. I wonder how this growth period has affected the initial composition of the community, and how many species may have been lost in the process. Do the authors have that information? Maybe not for all samples as this would be a lot. Can the authors maybe elaborate about why they chose to carry out such initial growth rather than re-suspending the sample in buffer and cryopreserving the sample directly?