The Hologenome Theory of Evolution

From MicrobeWiki, the student-edited microbiology resource
Revision as of 03:29, 11 May 2011 by MartinR (talk | contribs)

Introduction

A summary table of the number of the estimated counts of microbial species associated with specific animal and plant species or microhabitats. Table created by Zilber-Rosenburg and Rosenburg (2008).


The hologenome theory is a postulate put forth in 2007 by Eugene Rosenberg and Ilana Zilber-Rosenburg stating that the object of genomic natural selection is not a single organism, but the organism and its microbial communities (Rosenburg et al., 2007). This theory was originally based on the pair’s observations of Vibrio shiloi-mediated bleaching of the coral Oculina patagonica (Rosenburg & Zilber-Rosenburg, 2008); since its first introduction, the theory has been promoted as a fusion of Lamarckism and Darwinism (Rosenburg, Sharon, and Zilber-Rosenburg, 2009) and expanded to all of evolution, not just that of corals (Rosenburg & Zilber-Rosenburg, 2011). Recent research by the Rosenburg lab suggests that commensal bacteria play a role in mate choice by the fruit fly, Drosophila melanogaster, further supporting the hypothesis that greater genetic trends are determined by symbiotic microbiota (Sharon et al., 2010).




The Hologenome Theory


The Holobiont

The idea of holobiont is certainly not new: this term was coined originally by Margulis and Foster in 1991, and later adopted into various parts of evolutionary biology. The holobiont was appropriated for use particularly in reference to the large symbiotic communities residing in coral reefs (Rowan, 1998), and internet searches for this term primarily return research on coral communities. In general, a holobiont is any organism and all of its associated symbiotic microbes, including parasites, mutualists, synergists, and amensalists (Rosenburg & Zilber-Rosenburg, 2011). This is the unit of selection in the hologenome theory. Gilbert et al. (2010) refer to the development of the holobiont via selection of symbionts as symbiopoiesis.


The Coral Probiotic Hypothesis: The Beginnings of the Hologenome Theory

The cycle of Vibrio shiloi infection and subsequent bleaching of Mediterranean corals. Figure from Rosenburg et al.(2007).


Corals are a symbiotic partnership of many different marine bacteria, archaea, and eukaryotes with the invertebrate coral structure (Kushmaro & Rosenburg, 1997). Bleaching, or the loss of photosynthetic zooxanthellae from corals, is detrimental to the reef environment, as it inhibits shoal development and decreases biological production in the shallow ocean (Slonczewski & Foster, 2011). The 1980s and 1990s saw multiple large-scale bleachings of coral across the world’s oceans, largely the result of increases in ocean temperature (Goreau et al., 2000). Research of the Mediterranean coral bleaching in the mid-1990s used Koch’s postulates to show that growth of Vibrio shiloi, a gamma-proteobacterium, on the coral was responsible for the death of the required zooxanthellae (Fine & Loya, 1995; Kushmaro & Rosenburg, 1997).


In 2006, the Rosenburg lab published a paper titled “The Coral Probiotic Hypothesis” in the Journal of Environmental Microbiology (Reshef et al., 2006). Drawing from Fine & Loya’s (1995) findings that the coral contained large populations of cyanobacteria in its calcium carbonate skeleton, and combining this with the knowledge that changes in populations of microbes can allow the entry and growth of pathogenic species (Bignardi, 1998), the Rosenburg lab hypothesized that changes in temperature would alter microbe populations. Following the lab’s past conclusions, Reshef et al. asserted that temperature-mediated changes in symbiont species makeup allowed the colonization of the coral by Vibrio shiloi, and thus permitted the bleaching (Kushmaro & Rosenburg, 1997). Taking into consideration their more recent research that showed the development of resistance within coral populations shortly after the worst bleaching event in 1998 (Goreau et al., 2000), Reshef et al. argued that the a change of microbial communities within the coral—due to natural selection pressures exerted by the change in temperature—was responsible for macroscale adaptation on the part of the whole coral (2006).


The Hologenome Theory

In the hologenome theory, natural selection works on the level of simple Mendelian genetics, but also on a bigger scale. Certain microbiota are selected for based on the host environment as well as the other types of microbiota present (Arumugam et al., 2011).

Because the microbes associated with the larger host are so intimately tied to the organism, changes in either host environment or microenvironments within the host can cause changes in microbial genomes (Erlich, Hiller, & Hu, 2008; Gilbert et al., 2010). Thus, the genome being selected is not simply the host’s, but the hologenome—the genes of all of the microbiota as well as those of the larger organism (Rosenburg, Sharon, & Zilber-Rosenburg, 2009).

Larmarckism vs. Darwinism


In his 1859 work, On the Origin of Species, Charles Darwin put forth the famous “survival of the fittest” hypothesis (Darwin, 2003). This argued that evolution occurred through environmental selection of favored traits within a genetically varied population. Though the theory was met with much criticism at the time, it has come to be accepted as an accurate model for evolutionary progress (“Darwin,” 2006).

During the same period, a French scientist named Jean-Baptise Lamarck published his book Philosophie Zoologique, which proposed that organisms were the result of spontaneous creation followed by slow evolution towards more complicated forms (Nelson, 1975). While this theory is largely discredited now based on Stanley Miller’s early earth experiments, which showed that complex molecules could assemble from simple ones, suggesting that organisms could evolve from long-term series of reactions of increasing complexity (Miller, 1953), Lamarck did have some theoretical points that—although once dismissed—fit well within Darwinian theory. These are:

(1)The theory of use and disuse: individuals within a species lose characteristics they don’t use and develop new characteristics they will use.

(2)The transfer of acquired characteristics through inheritance: new characteristics within a species will be passed from parent to child (Rosenburg & Zilber-Rosenburg, 2009).


Later arguments by August Weismann, who said that only germ cells—which do not transmit newly acquired traits—were the mechanism of inheritance, and Mendel, whose genetics experiments suggested that variation was the result of random mutation within the population, caused the dismissal of Lamarckian theory from biological memory until recently (Mayr, 1985; Rosenburg & Zilber-Rosenburg, 2009). In 1983, Buss argued against the idea of germ cells being the sole unit of selection in his article, "Evolution, Development, and the Units of Selection", which cited key evidence that somatic cells could also transfer genetic information, particularly in fungi, protists, and plants, not to mention animals. Subsequent new research has shown that evolution is not simply a product of germ cell genes: DNA methylation, and RNAi, for example, alter the expression of genetic code based on environmental signals (Slonczewski & Foster, 2011).

While the Lamarckian principles of “use and disuse” and inheritance cannot be exemplified under the theory of simple host-organism Mendelian genetics, they can be shown within the holobiont. For example, increases in certain strains of symbiotic bacteria, if looking at the hologenome, count as gene amplifications, since each new bacterium carries copies of the bacterial genome. In this case, changes in environment cause changes in microbial communities that are transmitted to the entire organism—potentially changing metabolism or causing a pathogenic state (Rosenburg & Zilber-Rosenburg, 2009; Ehrlich, Hiller, & Hu, 2008; Gilbert et al., 2010). With changes in environment that change use of certain microbes by the host, then, we see a direct increase or decrease of the microbial population, which, in terms of the holobiont, is equivalent to changes in gene prevalence.

The same “use and disuse” strategy can be seen in the acquisition of new microbes from the environment. When new microbes are present in the host organism, they are either outcompeted by existing symbionts (“disuse”) or they outcompete (“use"). In this latter case, the new microbes establish residence within the host; when this occurs, their genomes become part of the hologenome of the host and its microbial partners (Zilber-Rosenburg & Rosenburg, 2008).

Schematic diagram of the interactions between living host and symbiotic microbiota. Figure from Fraune and Bosch (2010).

Though once inheritance of microbiota was deemed impossible due to the “Weismann barrier,” which held that germ cells were sole vehicles of heredity (Buss, 1983; Rosenburg & Zilber-Rosenburg, 2009), this is no longer found to be the case. Indeed, the easiest place to see this is the eukaryotic chloroplast or mitochondrion, which are maternally inherited degenerate alpha-proteobacterial endosymbionts (Dimijian, 2000). In addition, many endosymbionts are passed via the oocytes to the offspring (Rosenburg & Zilber-Rosenburg, 2009). In mammals, many endosymbionts are transmitted through infant contact with the birth canal or through breast milk (Martens, Chiang, & Gordon, 2008; Hehemann et al., 2010). In many plants (and some animals), vegetative reproduction uses somatic cells rather than gametes to form offspring; in this case, the offspring will gain any mutations acquired by the body cells (Rosenburg & Zilber-Rosenburg, 2009).

None of this is to say, however, that the hologenome theory does not fit within the Darwinian understanding of evolution. To the contrary, evolutionary process may be seen as “survival of the fittest” in which it is the whole organism—the host plus its "tagalong" microbes—that is being selected for. This theory allows for the rapid gain and loss of helpful traits, since microbial genomes are generally smaller, more easily mutated, and more rapidly transmitted—through vertical or horizontal transmission—than those of larger organisms (Slonczewski & Foster, 2011).

Examples of the Hologenome Theory at Work


Microbial Symbionts' Effects on Human Fitness

Human Microbiome Project phylogenetic map of the human holobiont. Tree taken from Zimmer (2010).

It has long been known that the presence of microbes is essential for human and animal development (Wostmann, 1981). However, it was only in recent years that the extent of microbes' effects on the human race was acknowledged and more carefully researched. In 2007, the NIH Common Fund began the Human Microbiome Project, an initiative whose focus was the sequencing of every symbiotic microorganism on the human body in order to gain a better understanding of the human holobiont ("Human Microbiome Project (HMP), 2007).

Recent research into the microbe's function in development has cited stimulation--and suppression--of the immune system as an important role of human symbionts (Mazmanian et al., 2005;Smits et al., 2005). Microorganisms have also been implicated in vitamin production, digestion, and angiogenesis in the human body (Slonczewski & Foster, 2011; Rosenberg & Zilber-Rosenberg, 2011). Mice born "germ-free" have longer digestion times and lower metabolic rates than those that have been normally colonized (Wostmann, 1981).

Perhaps the most essential role of microbiota, though, is not their direct contributions to the human body, but rather the protection that they offer against the growth of pathogens.

Microbes' Influence on Mate Selection in Drosophila melanogaster

The production of pheromones by the Drosophila melanogaster holobiont. Table created by Sharon et al. (2010).


In 2010, Sharon et al. announced that flies raised on specific media—either molasses or starch—tended to mate with those of the same past. However, when these flies were treated with antibiotics attacking gut microbiota, this preference was eliminated (Sharon et al., 2010). Previous studies have shown that microbiota vary with diet (Rosenburg & Zilber-Rosenburg, 2009), and that changes or absences of microbes in large eukaryotic organisms causes decreased fitness and loss of important social and reproductive traits (Singh, et al., 1990; Fraune & Bosch, 2010). Sharon et al. suggest that the changes in mating patterns are due to alterations in the Drosophila sex pheromones modified or secreted directly by the microbes inhabiting the fly (2010).

The reason for the mating preference in the first place, however, is not apparent, and Sharon et al. do not address this. While the paper argues that the preference for flies with the same eating habits—and theoretically, then, the same geographic location—minimizes intergroup mingling and encourages speciation, the reason for this being preferable is not apparent. In many cases, the purpose of sexual reproduction seems to be production rather than minimization of genetic variation, particularly when mating within your own group is likely to produce incestuous relationships. This is the case with human females, at least, who are entirely unattracted to the scents from those related to them (Andreae & Younger, 2009).

Conclusion


While the hologenome theory is still under contestation (Leggat et al. 2007; Rosenburg et al., 2007), it has gained some popularity within the scientific community as a way of explaining quick changes in adaptation that cannot be justified with traditional Darwinian thought. The holobiont, originally the designation for hard-to-quantify coral communities, has, in some eyes, at least, become the major unit of natural selection within the larger environment.

References

(1) Rosenburg, Eugene, Omry Koren, Leah Reshef, Rotem Efrony, and Ilana Zilber-Rosenburg. 2007. The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology 5: 355-362.

(2) Rosenburg, Eugene, and Ilana Zilber-Rosenburg. 2008. From bacterial bleaching to the hologenome theory of evolution. Proceedings of the 11th Annual Coral Reef Symposium Session 9: 269-273.

(3) Rosenburg, Eugene, Gil Sharon, and Ilana Zilber-Rosenburg. 2009. Opinion: The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environmental Microbiology 11(12): 2959-2962.

(4) Rosenburg, Eugene, and Ilana Zilber-Rosenburg. 2011. Symbiosis and Development: The Hologenome Concept. Birth Defects Research (Part C) 93: 56-66.

(5) Sharon, Gil, Daniel Segal, John M. Ringo, Abraham Hefetz, Ilana Zilber-Rosenburg, and Eugene Rosenburg. 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. PNAS 107(46): 20051-20056.

(6) Zilber-Rosenburg, Ilana, and Eugene Rosenburg. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. Federation of European Microbiological Societies Microbiology Review 32: 723-735.

(7) Kushmaro, A., and E. Rosenburg. 1997. Bleaching of the coral Oculina patagonica by Vibrio AK-1. Marine Ecology Progress Series 147: 159-165.

(8) Slonczewski, Joan, and John W. Foster. 2011. Microbiology: An Evolving Science. W. W. Norton & Co, New York, 1097 pages.

(9) Fine, M., and Loya, Y. 1995. The coral Oculina Patagonica: A new immigrant to the Mediterranean coast of Israel. Israel Journal of Zoology 41: 81.

(10) Bignardi, G. E. 1998. Risk factors for Clostridium difficile infection. Journal of Hospital Infections 40(1): 1-15.

(11) Goreau, Tim, Tim McClanahan, Ray Hayes, and Al Strom. 2000. Conservation of Coral Reefs after the 1998 Global Bleaching Event. Conservation Biology 14(1): 5-15.

(12) Reshef, Leah, Omry Koren, Yossi Loya, Ilana Zilber-Rosenburg, and Eugene Rosenburg. 2006. The Coral Probiotic Hypothesis. Environmental Microbiology 8(12): 2068-2073.

(13) Margulis, Lynn, and Renée Fester. 1991. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. MIT Press, Boston, 454 pages.

(14) Rowan, Rob. 1998. Review: Diversity and ecology of zooxanthellae on coral reefs. Journal of Phycology 34: 407-417.

(15) Gilbert, Scott F., Emily McDonald, Nicole Boyle, Nicholas Buttino, Lin Gyi, Mark Mai, Neelakantan Prakash, and James Robinson. 2010. Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philosophical Transactions of the Royal Society 365: 671-678.

(16) Ehrlich, Garth D., N. Luisa Hiller, and Fen Ze Hu. 2008. What makes pathogens pathogenic. Genome Biology 9(6): 225.

(17) Darwin, Charles. 2003. On the Origin of Species by Means of Natural Selection. Joseph Carroll, ed. Broadview Press, Calgary, 672 pages.

(18) “Darwin.” 2006. The American Museum of Natural History. New York, NY. <http://www.amnh.org/exhibitions/darwin/>

(19) [http://www.jstor.org/stable/4025218, Nelson, Gareth. 1975. Reviewed work(s): Inedits de Lamarck. D'apres les Manuscrits Conserves a la Biblioteque Centrale du Museum National d'Histoire Naturelle de Paris. by M. Vachon; G. Rousseau; Y. Laissus. Systematic Zoology 24 (2): 271-275.]

(20) Miller, Stanley. 1953. A production of amino acids under possible primitive Earth conditions. Science 117(3046): 528-529.

(21) Dimijian, Gregory D. 2000. Evolving together: the biology of symbiosis, part 2. Baylor University Medical Center Proceedings 13(4): 381-390.

(22) Martens, E.C., Chiang, H.C. & Gordon, J.I. 2008. Mucosal Glycan Foraging Enhances Fitness and Transmission of a Saccharolytic Human Gut Bacterial Symbiont. Cell Host & Microbe 4: 447-457.

(23). Hehemann, Jan-Hendrik, Gaëlle Correc, Tristan Barbeyron, William Helbert, Mirjam Czjzek, and Gurvan Michel. 2010. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464: 908-915.

(24) Singh, Prim B., Jeff Herbert, Bruce Roser, Lindsey Arnott, David K. Tucker, and Richard E. Brown. 1990. Rearing rats in a germ-free environment eliminates their odors of individuality. Journal of Chemical Ecology 16(5): 1667-1682.

(25) Fraune, Sebastian, and Thomas C. G. Bosch. 2010. Why bacteria matter in animal development and evolution. Bioessays 32: 571-580.

(26) Andreae, Simon, and James Younger. 2009. The Science of Sex Appeal. The Incubator, Film.

(27) Leggat, William, Tracy Ainsworth, John Bythell, Sophie Dove, Rught Gates, Ove Hoegh-Guldberg, Roberto Iglesias-Prieto, and David Yellowlees. 2007. The hologenome theory disregards the coral holobiont. Nature Reviews Microbiology 5: Online Correspondence. (nrmicro1635C1.)

(28) Rosenburg, Eugene, Omry Koren, Leah Reshef, Rotem Efrony, and Ilana Zilber-Rosenburg. 2007. The hologenome theory disregards the coral holobiont: reply from Rosenburg et al. Nature Reviews Microbiology 5: Online Correspondence. (nrmicro1635C2.)

Edited by Rachel Martin, student of Joan Slonczewski for BIOL 238 Microbiology, 2011, Kenyon College.