Eugene Rosenberg - Microbiomes: Current Knowledge and Unanswered Questions

The great scientific news that greeted this century was the campaign to decode the human genome. We must now remind ourselves that much of the biological composition of our bodies consists of genomes other than the human. Multitudes of bacteria and viruses occupy our skin, our mucous membranes, and our intestinal tract. They are likely to play a much larger role in developingand resistingdisease than we realize. Understanding this cohabitation of genomes within the human bodywhat I call the microbiomeis central to understanding the dynamics of health and disease.

Joshua Lederberg (2004)

We are in the midst of a paradigm change in biology. Plants and animals, including humans, can no longer be considered individuals, but rather, all are holobionts consisting of complex interactions between the host and abundant and diverse symbiotic microorganisms. During the last two decades, numerous studies have demonstrated that these symbionts play a critical role in many functions of macroorganisms, including metabolism, behavior, development, adaptation, and evolution (Gilbert et al. 2012; McFall-Ngai et al. 2013). Thus, individual phenotypes result from the combined expression of the host and microbiome genomes, leading to the popularization of notions of the holobiont and the hologenome (Zilber-Rosenberg and Rosenberg 2008; Rosenberg and Zilber-Rosenberg 2013, 2018).

I would like to mention briefly how Ilana Zilber-Rosenberg and I came upon the hologenome concept. In 1996, we discovered bacterial bleaching of corals (Kushmaro et al. 1996, 1997). After six years of studying the mechanisms of infection (reviewed in Rosenberg and Falkovitz 2004), we observed that the coral had become resistant to infection and bleaching by the specific coral pathogen, Vibrio shiloi. Because corals possess a restricted adaptive immune system and do not produce antibodies, we presented the coral probiotic hypothesis (Reshef et al. 2006) to explain the coral development of resistance to infection by V. shiloi. The hypothesis posits that the corals acquired beneficial bacteria from the marine environment that prevented infection by the pathogen. If it is possible to have epidemics of pathogens, why is it not possible (even more likely) to have epidemics of beneficial bacteria? They simply generally go unnoticed. Subsequently, we published data that support the coral probiotic hypothesis (Mills et al. 2013). A dynamic relationship exists between symbiotic microorganisms and corals under different environmental conditions that selects for the most advantageous coral holobiont in the context of the prevailing conditions.

Although the coral probiotic hypothesis inspired the hologenome concept, the concept was developed by consideration of the vast amount of data published by others. I especially acknowledge Forest Rohwer, whose pioneer article on the coral holobiont had a strong influence on us (Rohwer et al. 2001), Jan Sapp, whose book, Evolution by Association: A History of Symbiosis, was a stimulating introduction into the subject (Sapp 1994), and Eva Jablonka and Marion Lamb for their stimulating book, Evolution in Four Dimensions, which argues that there is more to heredity than genes (Jablonka and Lamb 2005).

In a previous book (Rosenberg and Zilber-Rosenberg 2013), we began by putting forth the hologenome concept of evolution. This was followed by a systematic review of the experimental evidence that existed at the time supporting the concept. This book takes a different approach. I first describe in some detail current knowledge of the properties of microbiomes, including their microbial abundance and diversity (Chap. discusses microbiomes in medicine and agriculture, including probiotics, prebiotics, synbiotics, fecal transplantation, and phage therapy. I conclude with a chapter on some philosophical and sociological implications of microbiome research.