Philobiblon

From A Symbiotic View of Life: We Have Never Been Individuals Author(s): Scott F. Gilbert, Jan Sapp and Alfred I. Tauber The Quarterly Review of Biology , Vol. 87, No. 4 (December 2012), pp. 325-341

p. 331 An instructive example comes from studies of the pea aphid, Acyrthosiphon pisum and the several species of bacteria that live in its cells: variants of Buchnera provide the aphid with thermotolerance (at the expense of fecundity at normal temperatures; Dunbar et al. 2007); Rickettsiella provides color change, turning genetically red aphids green through the synthesis of quinones (Tsuchida et al. 2010); and some variants of Hamiltonella provide immunity against parasitoid wasp infection (Oliver et al. 2009). But in the last case, the protective variants Hamiltonella result from the incorporation of a specific lysogenic bacteriophage within the bacterial genome. The aphid must be infected with Hamiltonella, and the Hamiltonella must be infected by phage APSE-3. As Oliver et al. (2009) write, “In our system, the evolutionary interests of phages, bacterial symbionts, and aphids are all aligned against the parasitoid wasp that threatens them all. The phage is implicated in conferring protection to the aphid and thus contributes to the spread and maintenance of H. defensa in natural A. pisum populations” (Oliver et al. 2009:994). But there is a cost to the host in having this beneficial protection, for in the absence of parasitoid infection, those aphids carrying the bacteria with lysogenic phage are not as fecund as those lacking them. Similarly, a tradeoff occurs in aphids that carry the thermotolerant genetic variants of Buchnera, i.e., while more heat resistant, they have less fecundity at milder temperatures than their sisters whose bacteria lack the functional allele for the heat-shock protein. However, the population as a whole can survive hot weather, which would otherwise prevent reproduction.

p. 332 The immune system may be formulated as having two “limbs”: an outward-looking limb that defines the organism as that which is to be protected from foreign pathogens, and an inward-looking arm that looks for potential dangers arising from within the organism itself (see Burnet and Fenner 1949; Tauber 2000, 2009; Ulvestad 2007; Eberl 2010; Pradeu 2010). This dualistic vision was the original conception of Metchnikoff at the end of the 19th century. He regarded immunity as a general physiology of inflammation, which included repair, surveillance for effete, dying, and cancer cells, as well as responsibility for the defense against invading pathogens (Tauber 1994). This larger, systemic understanding thus places defensive properties as only part of a continuous negotiation of numerous interactions between the organism and its biotic environment—both “internal” and “external” (Ulvestad 2007; Tauber 2008a,b). If the immune system serves as the critical gendarmerie keeping the animal and microbial cells together, then to obey the immune system is to become a citizen of the holobiont. To escape immune control is to become a pathogen or a cancer. In cancer, such autonomously proliferating (lower-level) cells must escape the innate, acquired, and anoikis-mediated immune systems of the host in order to survive (Hanahan and Weinberg 2011; Buchheit et al. 2012). Infections are those microbes that have similarly evaded the immuneenforced social modes of conformity (Hoshi and Medzhitov 2012).

p. 333 . To use an anthropomorphic analogy, the immune system is not merely the body’s “armed forces.” It is also the “passport control” that has evolved to recognize and welcome those organisms that help the body.,,, ” From this vantage, there is no circumscribed, autonomous entity that is a priori designated “the self.” What counts as “self” is dynamic and contextdependent.

p. 334 We are genomic chimeras: nearly 50% of the human genome consists of transposable DNA sequences acquired exogenously (Lander et al. 2001; Cordaux and Batzer 2009), possibly by the horizontal gene transfer from microbial symbionts to animal cells (see Dunning Hotopp et al. 2007; Altincicek et al. 2012). Although much of this added DNA is thought to be “parasitic,” some transposable elements may have been critical in creating new patterns of transcription (Sasaki et al. 2008; Oliver and Greene 2009; Kunarso et al. 2010). The emergence of the uterus, the defining character of eutherian mammals, appears to have been facilitated independently in several mammalian families by transposons integrating into the regions controlling the expression of the prolactin gene. These transposons contain transcription factor binding sites that enable the prolactin gene to become expressed in the uterine cells (Lynch et al. 2011; Emera et al. 2012). Moreover, this convergent evolution of gene expression via the insertion of transposable elements also suggests that such transposons can mediate adaptive evolution. The selective silencing of such transposons by DNA methylation or small interfering RNAs appears to be another policing mechanism that has facilitated evolution (Chung et al. 2008; Kaneko-Ishino and Ishino 2010; Castan˜eda et al. 2011). Thus, animals can no longer be considered individuals in any sense of classical biology: anatomical, developmental, physiological, immunological, genetic, or evolutionary. Our bodies must be understood as holobionts whose anatomical, physiological, immunological, and developmental functions evolved in shared relationships of different species. Thus, the holobiont, with its integrated community of species, becomes a unit of natural selection whose evolutionary mechanisms suggest complexity hitherto largely unexplored. As Lewis Thomas (1974:142) commented when considering self and symbiosis: “This is, when you think about it, really amazing. The whole dear notion of one’s own Self—marvelous, old free-willed, free-enterprising, autonomous, independent, isolated island of a Self—is a myth.”

p. 335

The milk oligosaccharides produced by human mothers cannot be utilized by newborn infants; however, they serve as an excellent food for strains of Bifidobacillus that enhance infant nutrition (Zivkovic et al. 2011). The vermiform appendix, long thought of as a vestigial organ, may actually serve as a reservoir for normal gut bacteria such that symbionts can be rapidly replaced after bouts of diarrhea (Smith et al. 2009). Diarrhea remains the leading cause of death in children of less-developed countries (CDC 2010), and antibiotic-induced colitis, caused by the spread of Clostridium after the normal symbionts have been killed, can be cured by the low-tech procedure of fecal transplants (usually from the spouse; Bakken 2011)

p. 335 , the possibility that microbes could regulate neural development had not been considered until recently. Now, however, a microbiota-gut-brain axis has recently been proposed (Cryan and O’Mahony 2011; McLean et al. 2012). Germfree mice, for example, have lower levels of NGF-1A and BDNF (a transcription factor and a paracrine factor associated with neuronal plasticity) in relevant portions of their brains than do conventionally raised mice. Heijtz et al. (2011:3051) have concluded that “during evolution, the colonization of gut microbiota has become integrated into the programming of brain development, affecting motor control and anxiety-like behavior.” In another investigation, a particular Lactobacillus strain has been reported to help regulate emotional behavior through a vagus nerve-dependent regulation of GABA receptors (Bravo et al. 2011). Investigations into the regulation of brain development by bacterial products were unthinkable before this challenge to the prevailing paradigm.

p. 336 This new paradigm for biology asks new questions and seeks new relationships among the different living entities on Earth. We are all lichens.