The microbial trafficking in genetic parts – within us

The prokaryotes (bacteria and archaea) that make up the majority of our microbial inhabitants (the microbiota) are known to engage in horizontal gene transfer (HGT) i.e., gene transfer among lineally unrelated individuals. The ‘holobiont’ perspective considers the human (or other macroscopic organism) and the associated microbial community as a composite organism. Can ecological and evolutionary considerations inform our analyses of gene transfer within the prokaryotic component of the microbiota, and do these analyses gain from a holobiontic perspective? This is the theme of my synthetic review published in Microbiome.

Nov 17, 2018
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There are more things in heaven and earth, Horatio,
Than are dreamt of in your philosophy.
- Hamlet  (Act 1, Scene 5, 167-8)

Humans harbor microbes in numbers comparable to that of their own cells [1].  This assemblage, specifically when considered as a unit of natural selection, has been termed as the (human) ‘holobiont’ [2].  Diverse microbial communities in various contexts exhibit horizontal genetic transfer (HGT) via a variety of mechanisms.  Horizontal, because this transfer of genetic material occurs among unrelated individuals, as opposed to vertical transfer through lines of descent.  Within the prokaryotic component of the microbiota, HGT can occur not only through the ‘classical’ modes – transformation, conjugation or transduction – but also via more recently discovered ones such as virus-like gene transfer agents, nanotubes, membrane vesicles and so on.  An incidental outcome of microbiome studies fueled by advances in high-throughput sequencing technologies is the realization that HGT can occur and be stabilized across phylogenetically distant groups of prokaryotes, especially under appropriate selection pressures. Several of these findings and possibilities for HGT are summarized in Fig. 1 (Fig. 2 in the paper).

Now, as the microbiome is part of the human holobiont, do these instances of HGT have consequences for the holobiont?  In my article, I have attempted to synthesize information from diverse sources that could have a bearing on this question.  Ever since Robert Koch conducted his seminal studies and formulated the germ theory of disease, we have studied microbes as pests rather than partners for a longer period of time.  Nevertheless, lurking in the data derived from the pests (decidedly a minuscule minority relative to their benign or indifferent kinsfolk) are tantalizing indications that aspects of human physiology can influence HGT among the resident microbiota that can, in turn, influence host physiology, again impacting HGT.  It is conceivable that such reciprocal influences result in the ‘tightening’ of the association of men and microbes.  By way of a case study, I have dwelt at some length on the chronic association between the stomach and duodenal ulcer-causing bacterium Helicobacter pylori and humans, its only known natural host.  Given the potential importance of such associations between humans (or other macroscopic organisms) and their resident microbiota, we suggest that the holobiontic perspective may be important in specific contexts.  However, other contexts may not require it, and may be effectively examined in the ‘traditional,’ reductionist standpoint of a microbial community in a given habitat, or even that of individual members of the community.

The above writing admittedly seems more ‘about the paper’ rather than something ‘behind’ it as this section would have you believe.  Not to disappoint, we make amends for our readers who take the time to access the article at Microbiome:  Mark Twain’s acerbic view of the microbial world and the mysterious ways of Providence at the beginning.  It also happens to be the only section that remained untouched by any criticism during the review process, and was not censured by the handling editor either.  

Note:  This article is part of the holobiont-themed collection titled "Host-microbiota interactions: from holobiont theory to analysis."

References:

1.  Sender R, Fuchs S, Milo R (2016) Revised Estimates for the Number of Human and Bacteria Cells in the Body. PLoS Biol 14(8): e1002533. https://doi.org/10.1371/journal.pbio.1002533

2.  Margulis L. Symbiogenesis and symbionticism. In: Margulis L, Fester R, editors. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. Cambridge: MIT; 1991. p. 1-14.

Disclaimer:  The opinions expressed herein do not represent the views of the TERI School of Advanced Studies or TERI.



Ramakrishnan Sitaraman

Professor, TERI School of Advanced Studies

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