In the Company of Microbes. Moselio Schaechter

observations seem at variance with the foregoing. First, there is the remarkable membrane compartmentation of a planctomycete bacterium like Gemmata obscuriglobus. However, three-dimensional reconstructions suggest that the visual compartments are due to a sectioned lobed conformation of an E. coli-reminiscent organism (Santarella-Mellwig et al. 2013), implicating a prokaryotic organization. Second, nuclei do not seem to be devoid of protein synthesis, though the nature of the proteins involved are not known (David et al. 2012). Presumably, an exception that might prove the rule.

       Nanne Nanninga is Emeritus Professor of Molecular Cytology, Swammerdam Institute for Life Sciences, University of Amsterdam, The Netherlands.

       References

      Madigan MT, Martinko JM, Parker J. 2003. Brock Biology of Microorganisms. 10th edition. Pearson Education, Inc., Upper Saddle River, NJ, USA.

      Byrne R, Levin JG, Bladen HA, Nirenberg MW. 1964. The in vitro formation of a DNA-ribosome complex. Proc Natl Acad Sci USA 52:140–148.

      David A, Dolan BP, Hickman HD, Knowlton JJ, Clavarino G, Pierre P, Bennink JR, Yewdell JW. 2012. Nuclear translation visualized by ribosome-bound nascent chain puromycylation. J Cell Biol 197:45–57.

      French SL, Santangelo TJ, Beyer AL, Reeve JN. 2007. Transcription and translation are coupled in Archaea. Mol Biol Evol 24:893–895.

      Lane N. 2011. Energetics and genetics across the prokaryote-eukaryote divide. Biol Direct 6:35.

      Martin W, Koonin EV. 2006. A positive definition of prokaryotes. Nature 442:868.

      Miller OL Jr, Hamkalo BA, Thomas CA Jr. 1970. Visualization of bacterial genes in action. Science 169:392–395.

      Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj IW, Devos DP. 2013. Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11:e1001565.

      Stanier RY, Van Niel CB. 1962. The concept of a bacterium. Arch Mikrobiol 42:17–35.

      Stent GS. 1966. Genetic transcription. Proc R Soc Lond B Biol Sci 164:181–197.

      November 2, 2014

       bit.ly/1RTn3q2

12

      The Microbial Nature of Humans

      by Maureen O’Malley

      Quite a lot has been written about human microbiome research and how it changes older ideas about human autonomy, individuality, and identity (e.g., Brüssow 2015; Hutter et al. 2014; Pradeu 2014). Most of these discussions focus on how the biological basis for our “self” is in fact a consortium of different lineages of cells, and that the majority of these cells are microbial. Microbiome research has revealed how particular compositional patterns in the microbial gut communities of humans are associated with phenotypic characteristics, such as disease states. Experiments in mice have added weight to interpretations that many of these associations are causal, and that the gut microbiota is the cause of multiple human phenotypes. Although the direction of causality is seldom clear and probably goes both ways, the potential phenotypic effects of microbes on human characteristics have reinforced even more strongly the notion of human identity as deeply microbial. Indeed, some literature might make a reader think that all that matters for any human characteristic is the gut microbiota in and of itself.

In a recent commentary, Harald Brüssow (2015) has raised the issue of whether “we are at a new level of defining human nature as a human-microbe consortium” (p. 13). He suggests this question can only be answered when there is stronger evidence for cooperative causal effects on human phenotypes of mutualistic members of our microbial communities. In other words, mutualism is defined by selective effects and not by accidental benefits (West et al. 2007). Only in such selected cooperative interactions, says Brüssow (p. 14), should we consider a microbial collective an “alter ego” of ourselves.

      This is a well-reasoned conclusion, and one that takes microbiome reflections beyond descriptive statistics of the numbers and relative proportions of microbes in the human body. Useful as such descriptions are, they are limited in what they say about the biological relevance of the microbiota. Consideration of selected cooperative relationships produces explanations of why these interactions matter, how they persist, and what the system under consideration actually is. Presumably, large numbers of the microbes in the human body fall by the explanatory wayside as “mere” commensals and adventitious parasites—large in number but not forming a “unit” that can be explained evolutionarily.

      Colorful shore of the Grand Prismatic Spring, Yellowstone National Park.

      Credit: Frank Kovalchek.

      Copyright. All rights reserved.

       https://www.flickr.com/photos/72213316@N00/3647773704

But does accepting an evolutionary explanation of some microbiota relationships really point to human “nature”? The idea of human nature is much disputed in philosophy, especially if it invokes anything like an essentialist natural kind (Kronfeldner et al. 2014). Kinds like this are not well regarded by micro- and other biologists, knowing what they do about biological variation and evolution. So Brüssow’s evolutionary criterion might be proposing an alternative viable definition of what human nature is: something determined by selected functional relationships with microbes inhabiting human bodies.

      Is this collective of human and microbiota a unit of selection in its own right? Unlike the integration of mitochondria (and later plastids) into what we now know as eukaryotic cells, the human body and its cooperative microbiota do not form a single unit of selection. The microbes retain reproductive autonomy, even if they rely on humans to provide a certain environment. Microbiota compositions are not strongly heritable either, although some of their functions may be. Humans reproduce separately from their microbes, and for the most part acquire them during and after birth. This separation of germ lines and lineages in time and space is usually the reason given for seeing humans and their microbiota–even the genuine mutualists—as separate Darwinian individuals or units of selection (Godfrey-Smith 2013).

Does this undermine the idea of humans as consortia of microbial and human cells? Only if being a Darwinian individual is the criterion for this designation. Instead, we might want to look at a spectrum of inevitable interactions with microbes, functional dependencies, and evolutionary persistent relationships. We know humans will not be germ-free except in the most extreme artificial situations. Some of these interactions will be beneficial and others harmful. Many of the most important interactions will not occur with microbes occupying the human gut or other bodily parts. Our place in the world comes with an obligation to interact with microbes at numerous levels, within and without our bodies. We depend on microbial by-products to survive, and we are nodes in larger webs of microbial interaction that define the planet. From this perspective, we are indeed “microbial”—inside, outside, and all around. Microbiome research has nudged our knowledge of ourselves so that we understand we occupy some peripheral node in this larger scheme, far from the center of biological interactions on the planet. Our node will eventually disappear, but the extinction of Homo sapiens will not lead to the collapse of the