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VI. Earth Life Emergence: Development of Body, Brain, Selves and Societies

4. Cellular Holobiont Symbiosis

    A good example of the independent principles in effect, via their discrete components, formative dynamics and modular division of labor, is the evolutionary occurrence of nucleated eukaryotic cells. Rather than due to gradual Darwinian trial and error, this further level of life came together and arose as diverse, mutually beneficial prokaryotic bacteria joined via advantageous symbiotic assemblies into bounded, whole entities. Disparate microbes provided mobility, digestion, oxygen tolerance and other functions which altogether formed a viable cellular unit. The pioneer researcher and valiant advocate since the 1970's of this now accepted understanding is Lynn Margulis (1938-2011), the late professor of microbiology at the University of Massachusetts, Amherst.


Again when this section went online in 2004, the presence of such a bacterial symbiosis was on the sidelines, often in question. As entries here, in Systems Evolution, and elsewhere attest, since circa 2012 this natural procreative propensity has become widely agreed upon as a main method by which life proceeded in its nested emergence. In the later 2010s, as noted by the title, due to Scott Gilbert, Jan Sapp, Seth Bordenstein, Joan Roughgarden, and other advocates, an integral perception of organisms, and our human selves, as a unitary microbiome of bacterial multitudes came to the fore. In regard, Ilana Zilber-Rosenberg and Eugene Rosenberg dubbed these symbiotic selves as holobionts to note their communal membership.

Earth, Life & System: An Interdisciplinary Symposium on Environment and Evolution in Honor of Lynn Margulis. www.depts.ttu.edu/vpr/faculty/scholarly-messenger/Downloads/ELSbookle.pdf. A conference in honor of the late Lynn Margulis, held at Texas Tech University, September 2012. The whole program with Abstracts is available at this website. Relevant speakers paid their respects to the founder and defender of the importance of symbiotic assemblies in life’s cellular origin and sustenance, and for consequent ecosystems from microbes to Gaia. For example, Jan Sapp spoke on “On the Origins of Biological Kingdoms and Domains,” Susan Squier gave “The ‘World Egg’ Reconsidered: Waddington, Margulis, and Feminist New Materialism,” Susan Oyama on “Sustainable Development: Alternative Pathways in Developmental Systems Theory” (see Abstract below), and Peter Westbroek’s “Coming to Terms with Global Change: Technology is Not Enough.” Geneticist James Shapiro’s paper “Bringing Cell Action into Evolution” is noted below.

“Sustainable development” is intentionally ambiguous; much of the talk is about multiple meanings within and outside biology. The developmental analog of that multiplicity is flexibility, whose importance in evolution will be explored. Some key terms will also get attention, including transmission, construction, interaction, and contingency. Contingency is often associated with chance or randomness, but the operative meaning here is causal dependency. Organisms are ontogenetically contingent; countless dependencies can be studied within the skin and extending out beyond it to an indefinite series of conditions and processes that are themselves contingent on other factors. Yet these densely interlocked and variable complexes can generate both the variation and the stability and recurrence needed for evolution. The discussion concludes with a consideration of sustainable development, intended not only in its usual contexts of agriculture and economic growth, but also in developmental and evolutionary studies. It is both possible and satisfying to see such regularity, when it occurs, in terms of interconnected systems of contingent influences. These last include symbiotic associations, among the most sustained, and sustaining, examples of long-term resource management we have. (Susan Oyama)

Individuals and Groups. www.icts.res.in/archive/program/details/315. As a May 2012 conference held at the G. B. Pant Institute of Himalayan Environment and Development, Uttarakhand, Almora, India, sponsored by the International Centre for Theoretical Sciences of the Tata Institute of Fundamental Research. A global gathering indeed as scientists and scholars such as Stuart Newman, Scott Gilbert, Ellen Clarke, Patrick Bateson, Paul Rainey travelled from afar to consider nature’s apparent penchant for symbiotic ensembles of autonomous entities in relational communities. In this new age of convergent integration, its self-organized universality is then seen to extend to, and spring from, chemical and physical grounds. Visit this site to view other Programs such as Quantitative Systems Biology, Physics of Life, Quantum Computation, and Mathematics of the Planet Earth.

A special issue of the Journal of Biosciences (39/2, April 2014), published by the Indian Academy of Sciences, contains a dozen presentations as a premier collection upon this organic reciprocity we would do well to implement. Vidyanand Nanjundiah and Newman introduce as “E Pluribus Unum” (Out of many, one). Gilbert again extols Symbiosis as the Way of Eukaryotic Life, while Rainey and Silvia De Monte wax on Nascent Multicellular Life and the Emergence of Individuality. Its substantial roots are traced in Group Behavior in Physical, Chemical and Biological Systems by Chian Saclioglu, et al, and An Ensemble Approach to the Evolution of Complex Systems by Goker Arpag and Ayse Erzan. A guide is the sequence of evolutionary transitions to individual entities, whence they are seen as nested communal reciprocities of wholes within Wholes. An historic precursor is the Arabic philosophy of Ibn Khaldun (1332-1406) in a paper by George Katsiaficas (search).

It is common in biology for more than one potential or actual unit of reproduction to form part of a larger whole that is composed of similar or dissimilar units. In many cases the whole displays group-level traits that are not seen in its constituents. One looks for explanations of a particular trait in terms of proximate causes, namely the underlying physics and chemistry, and separately in terms of the evolutionary history of the group. We will begin with overviews of how the individual versus group distinction is tackled in physics and chemistry. Next, different levels of biological organisation will be considered ranging from molecules to genes, proteins, metabolic pathways, cells, organisms and ecological communities. The phenomena to be examined will include collective oscillations, the reliability and stability of genetic and metabolic networks, multicellular development, normal and pathological social behaviour among cells and organisms and, finally, multi-species interactions. At least two talks will be devoted to the history of the concept of individuality. (Conference Abstract)

Molecular analyses of symbiotic relationships are challenging our biological definitions of individuality and supplanting them with a new notion of normal part–whole relationships. This new notion is that of a ‘holobiont’, a consortium of organisms that becomes a functionally integrated ‘whole’. This holobiont includes the zoological organism (the ‘animal’) as well as its persistent microbial symbionts. This new individuality is seen on anatomical and physiological levels, where a diversity of symbionts form a new ‘organ system’ within the zoological organism and become integrated into its metabolism and development. Symbionts have also been found to constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. We develop, grow and evolve as multi-genomic consortia/teams/ecosystems. (Gilbert Abstract)

Groups exhibit properties that either are not perceived to exist, or perhaps cannot exist, at the individual level. Such ‘emergent’ properties depend on how individuals interact, both among themselves and with their surroundings. The world of everyday objects consists of material entities. These are, ultimately, groups of elementary particles that organize themselves into atoms and molecules, occupy space, and so on. It turns out that an explanation of even the most commonplace features of this world requires relativistic quantum field theory and the fact that Planck’s constant is discrete, not zero. Groups of molecules in solution, in particular polymers (‘sols’), can form viscous clusters that behave like elastic solids (‘gels’). Group behaviour among cells or organisms is often heritable and therefore can evolve. This permits an additional, typically biological, explanation for it in terms of reproductive advantage, whether of the individual or of the group. (Saclioglu, et al Abstract)

Proto Tista. www.prototista.org. An extensive scientific website with topical introductions to symbiogenesis, Gais, emergence, self-organization, chaos, fractals, autopoiesis, among other similar realms.

Albert, Reka. Scale-Free Networks in Cell Biology. Journal of Cell Science. 118/4947, 2005. The fields of genomics, transcriptomics and proteomics are providing a vast quantity of intracellular molecular data, which can now be mapped by interaction graphs. These structures are not random but take on the dynamic geometry of invariant, redundant relationships as seen everywhere else. With the many internal components of a cell being identified and interrelated, the presence of a universal interconnectivity becomes evident. A prime feature is a nested, hierarchical modularity of nets within nets. An editorial for this issue avers that a challenge for the new cell biology, set forth in a turn of the millennium editorial (113/749): ….to go beyond ‘toon’ (diagram) explanations, to understand the emergent, self-organizing properties of interdependent systems, is being fulfilled by such as the subject article. As a reflection, these advances, as they integrate the many cellular particles and pieces, via a collaborative humankind, they contribute to a cosmic Copernican Revolution from moribund machine to organic genesis. For a popular update, see "Networks in Motion" by Albert and Adilson Motter in Physics Today, April 2012.

The architectural features of molecular interaction networks are shared to a large degree by other complex systems ranging from technological to social networks. (4953)

Allen, John and John Raven, eds. Introduction. Philosophical Transactions of the Royal Society of London B. 358/59, 2003. Chloroplasts and Mitochondria: Functional Genomics and Evolution is the topic of this issue. Based on Royal Society Discussion Meetings, many papers here consider “new perspectives on symbiosis in cell evolution.” In this regard a Russian Doll model is adopted to best express how these bacterial compartments nest within plant and animal cells so as to convert energy for photosynthesis and respiration.

Aon, Miguel, at al. Percolation and Criticality in a Mitochondrial Network. Proceedings of the National Academy of Sciences. 101/4447, 2004. Researchers at the Institute of Molecular Cardiobiology at Johns Hopkins University find complex system phenomena to explain the dynamic vitality of heart cells, cited as one more example of its universal instantiation.

We have recently observed that coordinated cell-wide oscillations in the mitochondrial energy state of heart cells can be induced by a highly localized perturbation of a few elements of the mitochondrial network, indicating that mitochondria represent a complex, self-organized system. (4447) The scaling and fractal properties of the mitochondrial network at the edge of instability agree remarkably well with the idea that mitochondria are organized as a percolation matrix, with reactive oxygen species as a key messenger. (4447)

Aon, Miguel, et al. The Scale-Free Dynamics of Eukaryotic Cells. PLoS One. 3/e3624, 2008. In work that would epitomize the systems biology turn and method, life scientists from the US, Canada, Japan, and the UK, find whole biological patterns and processes to be suffused by complexity, network phenomena which display in an invariant iteration.

Temporal organization of biological processes requires massively parallel processing on a synchronized time-base. We analyzed time-series data obtained from the bioenergetic oscillatory outputs of Saccharomyces cerevisiae and isolated cardiomyocytes utilizing Relative Dispersional (RDA) and Power Spectral (PSA) analyses. These analyses revealed broad frequency distributions and evidence for long-term memory in the observed dynamics. Moreover RDA and PSA showed that the bioenergetic dynamics in both systems show fractal scaling over at least 3 orders of magnitude, and that this scaling obeys an inverse power law. Therefore we conclude that in S. cerevisiae and cardiomyocytes the dynamics are scale-free in vivo. We argue that the operation of scale-free bioenergetic dynamics plays a fundamental role to integrate cellular function, while providing a framework for robust, yet flexible, responses to the environment. (Abstract excerpts)

Archibald, John. One Plus One Equals One: Symbiosis and the Evolution of Complex Life. Oxford: Oxford University Press, 2014. A few years after the passing of Lynn Margulis (1938-2011) a Dalhousie University, Nova Scotia, research professor of molecular biology praises in a book-length exposition her lifetime advocacy, against much resistance, of ubiquitous cellular mutualities amongst diverse microbes. Along with some other notices, the story can be told about how pervasive natural symbiotic assemblies actually are, which are now gaining inclusion in revised evolutionary theories.

Barbieri, Marcello. How Did the Eukaryotes Evolve? Biological Theory. Online February, 2017. The University of Ferrera biologist (search) continues his pioneer, innovative conception of evolution and living systems as most distinguished by many organic codes in effect beyond just genomes. For example, prokaryote bacteria are seen to form nucleated cells by way of signal transduction, splicing, tubulin, histone, cytoskeleton, compartment, and sequence codes, which serves to admit a pervasive biosemiotic essence.

Blackstone, Neil and Jeff Golladay. Why Do Corals Bleach? Conflict and Conflict Mediation in a Host/Symbiont Community. BioEssays. 40/8, 2018. Northern Illinois University biologists describe an on-going contest between relative entities and their local situation in the wider reef. We note for its value, and to report how symbiotic effects are being found and factored in everywhere. See also Hydra Regeneration Rethinking the Role of the Nervous System: Lessons from the Hydra Holobiont by Alex Klimovich and Thomas Bosch in this journal (online July 2018).

Coral bleaching has attracted considerable study, yet a question remains: given that corals and their Symbiodinium symbionts have co‐evolved for millions of years, why does this maladaptive process occur? Bleaching may result from evolutionary conflict between the host corals and their symbionts. Selection at the level of the individual symbiont favors using the products of photosynthesis for selfish replication, while selection at the higher level favors using these products for growth of the entire host/symbiont community. Fundamental features of photosynthesis have been co‐opted into conflict mediation so that symbionts that fail to export these products produce high levels of reactive oxygen species and undergo programmed cell death. These mechanisms function under most environmental conditions, but under conditions particularly detrimental to photosynthesis, it is these mechanisms of conflict mediation that trigger bleaching. (Abstract)

Bordenstein, Seth. Genomic and Cellular Complexity from Symbiotic Simplicity. Cell. 158/1236, 2014. A commentary on an article in the same issue, Sympatric Speciation in a Bacterial Endosymbiont by James Van Leuven, et al, whence pervasive “mutualisms” reveal the “power of nonadaptive forces in shaping organismal complexity.” The more that biologists study symbiotic microorganisms and their vast influences on animals, the more nature’s netwworkism unfolds is a continuum as different biological scales. As the late Lynn Margulis advocated for decades, the presence of beneficial symbiotic assemblies is now recognized as a major agency in evolution and life.

Bordenstein, Seth and Kevin Theis. Host Biology in Light of the Microbiome. PLoS Biology. Online August, 2015. We cite this paper by Vanderbilt University and University of Michigan biologists as a companion to the Symbioses Becoming Permanent colloquium (PNAS 112/Issue 33, 2015, search O’Malley) as evidence how well accepted the evolutionary and organismic presence of symbiotic assembles has become. In each case, much due is given to its valiant founder Lynn Margulis, who advocated this theory under much attack since the 1970s. Sadly she passed in 2011 and did not live to see its vindication. The main content here is Ten Principles of Holobionts and Their Hologenomes, as explained in the quotes. To sample, such occasions as eukaryotic, nucleated cells are “units of biological organization, comprehensive gene systems, Lamarkian due to environmental influences, supportive of multilevel selection,” and so on. But while a vital expansion of the evolutionary synthesis is in order, these insights are not seen to refute it. It ought to be noticed, however, that so many of these current advances, whether genomes, organisms, or brains (neuromes), involve additions of the interactive network connections between 20th century parts, be they genes, cells, or neurons.

Groundbreaking research on the universality and diversity of microorganisms is now challenging the life sciences to upgrade fundamental theories that once seemed untouchable. To fully appreciate the change that the field is now undergoing, one has to place the epochs and foundational principles of Darwin, Mendel, and the modern synthesis in light of the current advances that are enabling a new vision for the central importance of microbiology. Animals and plants are no longer heralded as autonomous entities but rather as biomolecular networks composed of the host plus its associated microbes, i.e., "holobionts." As such, their collective genomes forge a "hologenome," and models of animal and plant biology that do not account for these intergenomic associations are incomplete. Here, we integrate these concepts into historical and contemporary visions of biology and summarize a predictive and refutable framework for their evaluation.

Specifically, we present ten principles that clarify and append what these concepts are and are not, explain how they both support and extend existing theory in the life sciences, and discuss their potential ramifications for the multifaceted approaches of zoology and botany. We anticipate that the conceptual and evidence-based foundation provided in this essay will serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology's subdisciplines. At a time when symbiotic microbes are recognized as fundamental to all aspects of animal and plant biology, the holobiont and hologenome concepts afford a holistic view of biological complexity that is consistent with the generally reductionist approaches of biology. (Abstract)

The term "holobiont" traces back to Lynn Margulis and refers to symbiotic associations throughout a significant portion of an organism's lifetime, with the prefix holo- derived from the Greek word holos, meaning whole or entire. Amid the flourishing of host microbiome studies, holobiont is now generally used to mean every macrobe and its numerous microbial associates, and the term importantly fills the gap in what to call such assemblages. Symbiotic microbes are fundamental to nearly every aspect of host form, function, and fitness, including in traits that once seemed intangible to microbiology: behavior, sociality, and the origin of species. The conviction for a central role of microbiology in the life sciences has been growing exponentially, and microbial symbiosis is advancing from a subdiscipline to a central branch of knowledge in the life sciences. (2)

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