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

4. Cellular Holobiont Symbiogenesis

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)

Bornstein, Judith, ed. Mutualism. New York: Oxford University Press, 2015. The University of Arizona editor is a premier researcher in this field for three decades. Her introductory chapter advises that this term and its vital biological and evolutionary import is much akin to, another way of citing, life’s pervasive symbiosis. A chapter of special interest to us is Mutualistic Networks by Jordi Bascompte and Jens Olesen which describes the dynamic interconnections that join mutual aiders and symbiont entities.

Mutualisms, interactions between two species that benefit both of them, have long captured the public imagination. Their influence transcends levels of biological organization from cells to populations, communities, and ecosystems. Mutualistic symbioses were crucial to the origin of eukaryotic cells, and perhaps to the invasion of land. Furthermore, the key ecosystem services that mutualists provide mean that they are increasingly being considered as conservation priorities, ironically at the same time as the acute risks to their ecological and evolutionary persistence are increasingly being identified. This volume, the first general work on mutualism to appear in almost thirty years, provides a detailed and conceptually-oriented overview of the subject. Focusing on a range of ecological and evolutionary aspects over different scales (from individual to ecosystem), the chapters in this book provide expert coverage of our current understanding of mutualism whilst highlighting the most important questions that remain to be answered.

Bosch, Thomas and David Miller. The Holobiont Imperative: Perspectives from Early Emerging Animals. Switzerland: Springer, 2016. Any multicellular organism must be considered a holobiont or meta-organism, a complex community of many prokaryotic, eukaryotic, and viral species, which have been and are being evolved. (3) A Kiel University, Germany invertebrate zoologist and a James Cook University, Australia coral reef ecologist endorse this rising realization that all manner of creatures and persons are actually composite microbial ecosystems. After introducing this revolution, Major Events in the Evolution of Planet Earth shows how symbiotic, genomic syntheses were evident from life’s first rudiments. Its formative presence is carried through from unicell to multicellular Metazoan animals. As Lynn Margulis long advocated, inclusive symbiosis can now be cast as a major evolutionary factor. With all this in place, a pervasive microbial modularity can be seen in procreative effect.

Any multicellular organism must be considered a holobiont or meta-organism, a complex community of many prokaryotic, eukaryotic, and viral species, which have been and are being evolved. (3) A Kiel University, Germany invertebrate zoologist and a James Cook University, Australia coral reef ecologist endorse this rising realization that all manner of creatures and persons are actually composite microbial ecosystems. After introducing this revolution, Major Events in the Evolution of Planet Earth shows how symbiotic, genomic syntheses were evident from life’s first rudiments. Its formative presence is carried through from unicell to multicellular Metazoan animals. As Lynn Margulis long advocated, inclusive symbiosis can now be cast as a major evolutionary factor. With all this in place, a pervasive microbial modularity can be seen in procreative effect.

Bosch, Thomas, et al. Evolutionary “Experiments” in Symbiosis. BioEssays. Online May, 2019. TB, University of Kiel, Karen Guillemin, University of Oregon, and Margaret McFall-Ngai, University of Hawaii propose novel ways to properly and fully perceive the breadth and depth of communal reciprocities that so distinguish the many phases of natural life.

Nature has given us an overwhelming diversity of animals to study, and recent technological advances have greatly accelerated the ability to generate genetic and genomic tools to develop model organisms for research on host–microbe interactions. With the help of such models the authors therefore hope to construct a more complete picture of the mechanisms that underlie crucial interactions in a given metaorganism (entity consisting of a eukaryotic host with all its associated microbial partners). As reviewed here, new knowledge of the diversity of host–microbe interactions found across the animal kingdom will provide new insights into how animals develop, evolve, and succumb to the disease. (Abstract)

Brodsky, Vsevolod. Direct Cell-cell Communication. Biological Reviews. 81/1, 2006. The veteran Russian developmental biologist here finds ultradian (daily) intercellular rhythms to be self-organized and as a result possess a fractal self-similarity across several scales of tissue and cell.

Brucker, Robert and Seth Bordenstein. Speciation by Symbiosis. Trends in Ecology and Evolution. Online April, 2012. Vanderbilt University biologists provide an update tutorial on the copious extent that pervasive symbiotic assemblies serve to facilitate evolutionary development. An extensive bibliography accompanies. Our dear departed founder and advocate of this insight Lynn Margulis would be pleased.

Bull, Lawrence. On the Evolution of Eukaryotes: Computational Models of Symbiogenesis and Multicellularity. Lectures on Mathematics in the Life Sciences. Volume 26, 1999. Theoretical reasons for the formation of self-organized cells.

Cavalier-Smith, Thomas. Origin of the Cell Nucleus, Mitosis and Sex: Roles of Intracellular Coevolution. Biology Direct. 5/7, 2010. The latest views from the Oxford University evolutionary biologist are accessible in full on this journal’s website.

The transition from prokaryotes to eukaryotes was the most radical change in cell organisation since life began, with the largest ever burst of gene duplication and novelty. According to the coevolutionary theory of eukaryote origins, the fundamental innovations were the concerted origins of the endomembrane system and cytoskeleton, subsequently recruited to form the cell nucleus and coevolving mitotic apparatus, with numerous genetic eukaryotic novelties inevitable consequences of this compartmentation and novel DNA segregation mechanism. Physical and mutational mechanisms of origin of the nucleus are seldom considered beyond the long-standing assumption that it involved wrapping pre-existing endomembranes around chromatin. Discussions on the origin of sex typically overlook its association with protozoan entry into dormant walled cysts and the likely simultaneous coevolutionary, not sequential, origin of mitosis and meiosis. (Abstract)

Chanson, Lea, et al. Self-organization is a Dynamic and Lineage-intrinsic Property of Mammary Epithelial Cells. Proceedings of the National Academy of Sciences. 108/3264, 2011. Researchers from the Ecole Polytechnique, LBNL, and UC Berkley, find self-organization to be a basic formative feature of communities of normal adult human cells, a property whose loss or reversal can signal a cancerous situation.

Chaston, John and Angela Douglas. Making the Most of “Omics” for Symbiosis Research. Biological Bulletin. 223/1, 2012. In a special issue “Discoveries in Animal Symbiosis in the “Omics” Age” as a memorial for the life and work of Lynn Margulis, Cornell University entomologists describe how 21st century capabilities for detailed analysis across life’s organismic evolution give further definitive credence to the presence and importance of such mutual reciprocities. The paper goes on to extol the ways that “omics” methods and insights are bringing novel vistas to biological understandings. One is then intrigued whether this approach can be expanded to imagine an “informomics,” and “cosmomics,” the list goes on, to express an innate uniVerse and uniVerve?

Omics, including genomics, proteomics, and metabolomics, enable us to explain symbioses in terms of the underlying molecules and their interactions. The central task is to transform molecular catalogs of genes, metabolites, etc., into a dynamic understanding of symbiosis function. We review four exemplars of omics studies that achieve this goal, through defined biological questions relating to metabolic integration and regulation of animal-microbial symbioses, the genetic autonomy of bacterial symbionts, and symbiotic protection of animal hosts from pathogens. As omic datasets become increasingly complex, computationally sophisticated downstream analyses are essential to reveal interactions not evident from visual inspection of the data. We discuss two approaches, phylogenomics and transcriptional clustering, that can divide the primary output of omics studies—long lists of factors—into manageable subsets, and we describe how they have been applied to analyze large datasets and generate testable hypotheses. (Abstract)

Chen, Irene and Peter Walde. From Self-Assembled Vesicles to Protocells. Cold Spring Harbor Perspectives in Biology. 2/7, 2011. Harvard and ETH, Zurich, systems biologists help affirm life’s constant propensity toward “compartmentalization,” the formation at every nested scale of bounded, whole entities from these primal precursors to all manner of cells, organisms, and on to cellular-like communities.

Self-assembled vesicles are essential components of primitive cells. We review the importance of vesicles during the origins of life, fundamental thermodynamics and kinetics of self-assembly, and experimental models of simple vesicles, focusing on prebiotically plausible fatty acids and their derivatives. We review recent work on interactions of simple vesicles with RNA and other studies of the transition from vesicles to protocells. Finally we discuss current challenges in understanding the biophysics of protocells, as well as conceptual questions in information transmission and self-replication.

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