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Systems biology of eukaryotic superorganisms and the holobiont concept

Abstract

The founders of modern biology (Jean Lamarck, Charles Darwin, August Weismann etc.) were organismic life scientists who attempted to understand the morphology and evolution of living beings as a whole (i.e., the phenotype). However, with the emergence of the study of animal and plant physiology in the nineteenth century, this “holistic view” of the living world changed and was ultimately replaced by a reductionistic perspective. Here, I summarize the history of systems biology, i.e., the modern approach to understand living beings as integrative organisms, from genotype to phenotype. It is documented that the physiologists Claude Bernard and Julius Sachs, who studied humans and plants, respectively, were early pioneers of this discipline, which was formally founded 50 years ago. In 1968, two influential monographs, authored by Ludwig von Bertalanffy and Mihajlo D. Mesarović, were published, wherein a “systems theory of biology” was outlined. Definitions of systems biology are presented with reference to metabolic or cell signaling networks, analyzed via genomics, proteomics, and other methods, combined with computer simulations/mathematical modeling. Then, key insights of this discipline with respect to epiphytic microbes (Methylobacterium sp.) and simple bacteria (Mycoplasma sp.) are described. The principles of homeostasis, molecular systems energetics, gnotobiology, and holobionts (i.e., complexities of host–microbiota interactions) are outlined, and the significance of systems biology for evolutionary theories is addressed. Based on the microbe—Homo sapiens—symbiosis, it is concluded that human biology and health should be interpreted in light of a view of the biomedical sciences that is based on the holobiont concept.

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Fig. 1

Portrait adapted from Locy (1915)

Fig. 2
Fig. 3

Adapted from Niklas and Kutschera (2015)

Fig. 4
Fig. 5
Fig. 6

Adapted from Schauer and Kutschera (2008)

Fig. 7

Adapted from Kleinig and Sitte (1986)

Fig. 8

Adapted from Follmann and Brownson (2009), updated 2018

Fig. 9
Fig. 10
Fig. 11

Adapted from Segre and Salafsky (2016)

Fig. 12

Adapted from a painting of Glynn Gorick, with permission of the artist

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Acknowledgements

I thank Dr. Steve Farmer (Chief Science Officer of the Systems Biology Group, Inc., CA, USA) for inviting me to visit his Institution to write this article, and for helpful comments on earlier versions of the manuscript. The cooperation between S. F. and U. K. was supported by the Alexander von Humboldt Foundation, Bonn, Germany (Stanford 2013/2014 to U. K., Institute of Biology, University of Kassel, Germany).

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Kutschera, U. Systems biology of eukaryotic superorganisms and the holobiont concept. Theory Biosci. 137, 117–131 (2018). https://doi.org/10.1007/s12064-018-0265-6

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Keywords

  • Evolution
  • Holobiont
  • Systems biology
  • Reductionism
  • Superorganism