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Prokaryotic Horizontal Gene Transfer Within the Human Holobiont: Ecological- Evolutionary Inferences, Implications and Possibilities Ramakrishnan Sitaraman

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Prokaryotic Horizontal Gene Transfer Within the Human Holobiont: Ecological- Evolutionary Inferences, Implications and Possibilities Ramakrishnan Sitaraman Sitaraman Microbiome (2018) 6:163 https://doi.org/10.1186/s40168-018-0551-z REVIEW Open Access Prokaryotic horizontal gene transfer within the human holobiont: ecological- evolutionary inferences, implications and possibilities Ramakrishnan Sitaraman Abstract The ubiquity of horizontal gene transfer in the living world, especially among prokaryotes, raises interesting and important scientific questions regarding its effects on the human holobiont i.e., the human and its resident bacterial communities considered together as a unit of selection. Specifically, it would be interesting to determine how particular gene transfer events have influenced holobiont phenotypes in particular ecological niches and, conversely, how specific holobiont phenotypes have influenced gene transfer events. In this synthetic review, we list some notable and recent discoveries of horizontal gene transfer among the prokaryotic component of the human microbiota, and analyze their potential impact on the holobiont from an ecological-evolutionary viewpoint. Finally, the human-Helicobacter pylori association is presented as an illustration of these considerations, followed by a delineation of unresolved questions and avenues for future research. Keywords: Microbiome, HGT, Lateral gene transfer, DNA transfer, Symbiont, Microbial ecology, Co-evolution, Natural selection, Host-microbe interaction, Helicobacter pylori were typhoid germs, and cholera germs, "Noah and his family were saved -- if that could be and hydrophobia germs, and lockjaw germs, and calledanadvantage.Ithrowinthe‘if’ for the consumption germs, and black-plague germs, and reason that there has never been an intelligent some hundreds of other aristocrats, specially person of the age of sixty who would consent to live precious creations, golden bearers of God’sloveto his life over again. His or anyone else’s. The Family man, blessed gifts of the infatuated Father to his were saved, yes, but they were not comfortable, for they children -- all of which had to be sumptuously were full of microbes. Full to the eyebrows; fat with housed and richly entertained; these were located in them, obese with them, distended like balloons. It was a the choicest places the interiors of the Family could disagreeable condition, but it could not be helped, furnish: in the lungs, in the heart, in the brain, in because enough microbes had to be saved to supply thekidneys,intheblood,intheguts.Intheguts thefutureracesofmenwithdesolatingdiseases, particularly. The great intestine was the and there were but eight persons on board to serve favorite resort. There they gathered, by countless bil- as hotels for them. The microbes were by far the lions, and worked, and fed, and squirmed, and sang mostimportantpartoftheArk’scargo,andthe hymns of praise and thanksgiving; and at night part the Creator was most anxious about and most when it was quiet you could hear the soft murmur infatuated with. They had to have good of it. The large intestine was in effect their heaven. nourishment and pleasant accommodations. There They stuffed it solid; they made it as rigid as a coil of gaspipe. They took pride in this. Their principal Correspondence: [email protected] hymn made gratified reference to it: Department of Biotechnology, TERI School of Advanced Studies, 10 Institutional Area, Vasant Kunj, New Delhi 110070, India © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sitaraman Microbiome (2018) 6:163 Page 2 of 14 Constipation, O Constipation, In the evolutionary context, natural selection acts dir- ectly on phenotypes and only indirectly on genotypes The Joyful sound proclaim [21]. Selection is blind to the underlying causes of a phenotype: It is merely sufficient to produce an advanta- Till man's remotest entrail geous phenotype in order to reap the benefits of in- creased fitness [22]. For example, the regulatory Shall praise its Maker’s name." networks underlying the control of mating type in phylogenetically close species of yeast may diverge sig- – Mark Twain, Letters from the Earth (1909) nificantly in terms of how individual genes are regulated but without affecting the final output of the network [23]. Likewise, functional convergence for carbohydrate catabolism observed in the human gut microbiota has Background been attributed to the cooperation of different microbial The human (or other multicellular host) with its symbi- species in different individuals [24] (see Fig. 1 and the otic microbiota is termed the ‘holobiont’—a term coined section ‘HGT driven by human diet: examples of envir- by Lynn Margulis [1]. The tenability the holobiont view onmental selection’ below). Furthermore, the possibility in the specific sense of its being a unit of selection was of neutral or nearly neutral evolutionary changes implies first elaborated by Zilber-Rosenberg and Rosenberg [2]. that the existence of a particular phenotype may not ne- Advocates of this view point to the importance and cessarily indicate its utility in terms of prior episodes of indispensability of the human-microbial symbiosis in selection or enable us to infer the nature of the selection multiple contexts—anatomical, genetic, physiological, that brought it about in every instance [25, 26]. As metabolic, developmental and immunological [3]. Critics Sydney Brenner put it, ‘biology, because of evolution, is of this view suggest that the majority of human-micro- only the art of the satisfactory’ [20]. All that we can say bial associations that develop after birth do not fulfill the with any certainty is that the evolution of multicellularity requisite criteria of vertical transmission and partner fi- among eukaryotes (with or without prokaryotic interven- delity [4, 5]. It was previously suggested that this process tion) opened up new ecological niches for other of microbial colonization commences via the placenta in organisms, especially prokaryotes, by serving as a con- utero itself [6], but subsequent studies attributed this centrated source of nutrients and a fairly stable habitat. finding to contamination [7]. Thus, colonization by ma- Current interactions between these two groups— ternal microbes commences during the passage through whether as commensals or mutualists or parasites or the birth canal and later through breast milk [8–13]. Hu- even facultative opportunists switching between com- man microbial communities undergo post-natal remod- mensalism and parasitism—offer few clues as to how eling and begin converging to the characteristic ‘adult’ these various relationships evolved and stabilized in the profile as early as age one [14, 15]. Had this associ- first instance. The acquisition, modulation and mainten- ation been entirely facultative, and both microbiota and ance of a characteristic microbiota by multicellular hosts host (especially the host) capable of elaborating ‘normal’ is probably evolutionarily ancient and conserved across phenotypes with little or no impact on the overall fitness, diverse lineages. Characteristic and conserved micro- there would be no conceptual or methodological advance biota are present even among representatives of basal in using the word ‘holobiont.’ However, rapidly accumulat- metazoan lineages such as sponges (Phylum Porifera) ing data in the field highlight the obligate nature of this [27–30] and Hydra vulgaris (Phylum Coelenterata) [31]. association for humans (and other multicellular organ- The fluctuations in microbial community composition in isms) in ensuring homeostasis over the holobiont’slifetime the initial stages of colonization in H. vulgaris involve (surveyed in [3]). For example, it has been observed that host modulation by anti-microbial peptides (AMPs) germ-free mice, though viable, exhibit various develop- resulting in the eventual stabilization of the assembled mental and immunological abnormalities [16–19]. We microbial communities over the lifetime of the host [32]. therefore suggest that one need not necessarily privilege Recent research based on analysis of the more rapidly the holistic view over a more reductionist view of the evolving gyrB gene, rather than the more slowly evolving holobiont as a collection of relatively autonomous inter- 16S rRNA gene, has uncovered evidence of co-speciation acting modules, especially because organisms and com- of gut microbiota within hominid lineages—humans, munities are indeed constructed on a modular plan [20]. chimpanzees, gorillas and bonobos. Specific clades of Bac- Rather, the holobiontic view is a reminder of a higher level teroidaceae and Bifidobacteriaceae identified by gyrB se- of complexity that we cannot afford to ignore if we are to quences have been maintained within these four hominid arrive at a more complete understanding of the working lineages over the order of ~ 105 generations [33]. However, of multi-organismal assemblages, including ourselves. the distribution of Lachnospiraceae indicated that lateral Sitaraman Microbiome (2018) 6:163 Page 3 of 14 Holobiont A Holobiont B Holobiont C
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