Flying solo; the tale of my plunge into community assembly.

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BioMed Central
BioMed Central BioMed Central

A conceptual framework for the phylogenetically constrained assembly of microbial communities - Microbiome

Microbial communities play essential and preponderant roles in all ecosystems. Understanding the rules that govern microbial community assembly will have a major impact on our ability to manage microbial ecosystems, positively impacting, for instance, human health and agriculture. Here, I present a phylogenetically constrained community assembly principle grounded on the well-supported facts that deterministic processes have a significant impact on microbial community assembly, that microbial communities show significant phylogenetic signal, and that microbial traits and ecological coherence are, to some extent, phylogenetically conserved. From these facts, I derive a few predictions which form the basis of the framework. Chief among them is the existence, within most microbial ecosystems, of phylogenetic core groups (PCGs), defined as discrete portions of the phylogeny of varying depth present in all instances of the given ecosystem, and related to specific niches whose occupancy requires a specific phylogenetically conserved set of traits. The predictions are supported by the recent literature, as well as by dedicated analyses. Integrating the effect of ecosystem patchiness, microbial social interactions, and scale sampling pitfalls takes us to a comprehensive community assembly model that recapitulates the characteristics most commonly observed in microbial communities. PCGs’ identification is relatively straightforward using high-throughput 16S amplicon sequencing, and subsequent bioinformatic analysis of their phylogeny, estimated core pan-genome, and intra-group co-occurrence should provide valuable information on their ecophysiology and niche characteristics. Such a priori information for a significant portion of the community could be used to prime complementing analyses, boosting their usefulness. Thus, the use of the proposed framework could represent a leap forward in our understanding of microbial community assembly and function.

Having recently finished a great period as Marie Sklodowska-Curie fellow working on viral Metagenomics, I was lucky enough to get an Assistant Professor position in my hometown. While the amount of bureaucratic and teaching work involved, especially in Spain, would surely take a toll in my scientific career, the opportunity was a godsend, as I had two kindergarten-aged girls, and a spouse that had already accompanied me previously overseas for a three years postdoc.

What interesting idea could I attack without much hope for initial funding or too much spare time, and on my own?. Actually, I knew exactly what I wanted to do, something that had been on the back of my mind for the last four years. During the last year of my first postdoc I analyzed human gut microbiota samples looking for bacterial groups present in all samples (i.e. core), something much en vogue at the time. I did not merely focus on a fixed OTU similarity clustering threshold or taxonomic rank, and indeed found various core groups. Not only did these core groups varied in phylogenetic depth, but their subsequent co-abundance network analysis revealed various intriguing features that did look to me (a likely biased observer) as hints of community assembly rules. Unfortunately, the results were based on too few samples and I finished my contract and was eager to move forth before we could find a larger dataset.

Now was the time to revisit those results. I carried out a similar analysis on large and comprehensive human gut datasets and found that they presented a preeminent compositional core comprised of discrete core groups of varying phylogenetic depth [1]. However, when I communicated my feeling that the existence of phylogenetic core groups in microbial ecosystems was a thread worth pulling from, many colleagues at conferences and meetings (and various reviewers) received the idea with a clear lack of enthusiasm and commonplace responses such as “the OTU is dead, you have to use ESVs”, “communities assemble based on functional genes, not bacterial groups” or “16S sequencing is the past, only shotgun metagenomics matters now”. I understood what they meant but felt that their commentaries were unrelated to my idea that given the fact that both microbial traits and ecological coherence show signs of phylogenetic conservation, the possible existence of phylogenetic core groups in microbial ecosystems was noteworthy. If I was a fool, what was I not seeing?

So, I set out to explain myself properly, read quite a bit, found inspiring papers (e.g. [2, 3]), and produced what I felt was a worthy conceptual framework for the assembly of microbial communities. The final factor that convinced me of its value was the discovery of Goldford et al. study of community assembly on single carbon and energy sources using complex microbial communities derived from different natural habitats [4]; my a priori theoretical predictions beautifully matched their experimental results!.

You can find my ideas on microbial community assembly published here:

 https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-019-0754-y

 

1.            Aguirre de Cárcer D. The human gut pan-microbiome presents a compositional core formed by discrete phylogenetic units. Scientific Reports. 2018;8:14069.

2.            Cordero OX, Datta MS. Microbial interactions and community assembly at microscales. Current Opinion in Microbiology. 2016;31:227-34.

3.            Kinnunen M, Dechesne A, Proctor C, Hammes F, Johnson D, Quintela-Baluja M et al. A conceptual framework for invasion in microbial communities. The Isme Journal. 2016;10:2773.

4.            Goldford JE, Lu N, Bajić D, Estrela S, Tikhonov M, Sanchez-Gorostiaga A et al. Emergent simplicity in microbial community assembly. Science. 2018;361:469-74.

 

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