I wrote an opinion piece called 'Applying the core microbiome to understand host-microbe systems', which I was luckily enough to publish in one of my fave journals, Journal of Animal Ecology. This idea stemmed from a discussion with reviewers of a paper I had submitted, where each of the reviewers and editors had a very specific (and often different) idea of what the core microbiome meant. The core microbiome has traditionally pertained to what are likely to be functional microbes within a microbial community, but given with a bit of imagination we can link almost any trait to 'function' (commonness, stability, keystoneness, etc), as well as the fact that 'function' has numerous definitions (although these can be split into two major conceptual groups, as nicely summarized by Klaassen 2018), this has lead to the concept of the core microbiome being extremely widely applied (at least in ecological fields), yet not very well defined. This lack of definition makes it relatively unpopular with pure microbiologists, I believe, who apply it far less frequently than ecologists, and generally think of the core in terms of functional genes rather than key taxonomic units. I had a look through the host-microbe special issues of Molecular Ecology and Journal of Animal Ecology from 2018 before I wrote the piece, and found 14 articles, out of all published across the two special issues, applied or referred to the core microbiome. I reckon that was about a third of all papers. In light of this, I started thinking about why the core microbiome always had to be about function. And when it IS about function, could we be a bit more specific about what sort of function we are talking about? It is well established now that common microbes are not necessarily functional to the host, whilst rare microbes can provide essential services (Jousset et al. 2017 is a nice review of this, although the focus is largely on free-living microbial systems), so the main tenet of the common core being functional is no longer correct (or at least, should definitely not be assumed). This is essentially stating the obvious for microbiologists, who sometimes consider the concept of the core more or less useless unless it stems from shotgun metagenomics data and is gene-based. Yet for ecologists, who are very much interested in organismal-level interactions, it makes sense to want to pick out some key microbes out of the thousands in their data sets. The question I tackle is the article is: key for what? The most common measure is spatial distribution among hosts (the 'common core'), which identifies 'key' microbes with respect to their prevalence (and/or abundance), yet this is arguably the least informative measure of a microbe's ecological role (at least by itself, in combination with other traits it can offer additional insights into its ecology). Some microbes may be particularly influential for the ecological processes that govern community stability and ecological co-occurrence and trophic networks, both of which may have indirect effects on host function (or not), but most likely act independently of host function. Gut microbiomes may particularly good for studying such processes since they represent relatively closed systems and well defined meta-communities compared to free-living microbiomes.
In terms of functional processes, I also outline why it's important to distinguish between microbes that have co-evolved with the host and those that are more likely to present faculative symbionts, which in my view are represented by the 'functional core' and the 'host-adapted core', respectively. Both types may identify functionally relevant microbes, but the evolutionary and ecological processes that maintain them are different. Namely, host-adapted microbes provide specific functional benefits that are not provided by other microbes, have an affect on host fitness (at least in some ecological contexts), and are actively encouraged to colonise by the host. Faculative microbes, however, also provide functional benefits to the host, but if such benefits can also be provided by many other phylogenetically unrelated microbes, there is little selection pressure for a symbiotic relationship to evolve. In the article I outline more specifically how these two can be distinguished, although it remains a big challenge! My conclusions after all this is that I think the concept of the core microbiome can be still be useful for ecologists, in that it can provide a framework of identifying key microbes within the host-associated microbiome, but that the processes for which they are 'key' for should be more explicitly defined.
3 Comments
Shabana Hoosein
13/4/2021 07:32:18 pm
A very much needed piece in understanding how the identification of core microbiota are interpreted by different fields based on the questions asked. Thank you! I can now point researchers to this paper when they give me baffled looks as I describe the core microbiome.
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Alice Risely
1/6/2022 11:24:38 am
Thanks! I somehow didn't see this comment before - so a bit of a late reply :)
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