A Symbiotic View of Life: We Have Never Been Individuals

Abstract

The notion of the "biological individual" is crucial to studies of genetics, immunology, evolution, development, anatomy, and physiology. Each of these biological subdisciplines has a specific conception of individuality, which has historically provided conceptual contexts for integrating newly acquired data. During the past decade, nucleic acid analysis, especially genomic sequencing and high-throughput RNA techniques, has challenged each of these disciplinary definitions by finding significant interactions of animals and plants with symbiotic microorganisms that disrupt the boundaries that heretofore had characterized the biological individual. Animals cannot be considered individuals by anatomical or physiological criteria because a diversity of symbionts are both present and functional in completing metabolic pathways and serving other physiological functions. Similarly, these new studies have shown that animal development is incomplete without symbionts. Symbionts also constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. The immune system also develops, in part, in dialogue with symbionts and thereby functions as a mechanism for integrating microbes into the animal-cell community. Recognizing the "holobiont"--the multicellular eukaryote plus its colonies of persistent symbionts--as a critically important unit of anatomy, development, physiology, immunology, and evolution opens up new investigative avenues and conceptually challenges the ways in which the biological subdisciplines have heretofore characterized living entities.

The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing

“…This is particularly true for symbioses between animals and microbes (Gilbert et al, 2012). The improved understanding is partly a result of the availability of high-throughput, culture-independent techniques of community surveys and partly a result of maturation of the field of symbiology.…”

Organisms or biological individuals? Combining physiological and evolutionary individuality

“…The conception of a biological individual as endogenous and autonomous must be rejected, but not the idea of a biological individual in general -contrary to what Gilbert et al (2012), for instance, have suggested. Quite the contrary, the immune system is pivotal to explain how entities of different origins can stick together and interact within a functional and cohesive whole (Sansonetti and Medzhitov 2009;Pradeu 2010;Chu and Mazmanian 2013).…”

Senomic view of the cell: SenomeversusGenome

“…Only such a focus and approach to these self-referential phenomena will allow us to fully understand their biological basis as well as their true non-genomic and primary nature. Since any viewpoint that the cell is a functional automaton no longer comports with scientific data, those sources of informational input and the complex mechanisms by which information is assessed, communicated, deployed and managed becomes the new ground state of any detailed understanding of cellular life or the holobionts that are its collective product [31,53]. As each biological organism is inevitably a subject, and its world-view is constructed internally from its particular self-referenced Senome evolved during its specific evolutionary trajectory and enfolded during its individual life, it is obvious that the Senome o f each organism is unique.…”