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

4. Cellular Holobiont Symbiogenesis

Norris, Vic and Robert Root-Bernstein. The Eukaryotic Cell Originated in the Integration and Redistribution of Hyperstructures from Communities of Prokaryotic Cells Based on Molecular Complementarity. International Journal of Molecular Sciences. 10/2611, 2009. A University of Rouen biologist and the Michigan State University psychologist expand the main view that cellular life originated due to discrete components such as nucleotides and bacteria alone. Rather, an integrational milieu, an ecological whole system, is in equal existence as it repeatedly served to self-organize such entities into this evolutionary procession. Robert Root-Bernstein has pursued this theme for over a decade and here achieves a robust update, see also Alex Hunding, et al, for further confirmation.

In the “ecosystems-first” approach to the origins of life, networks of non-covalent assemblies of molecules (composomes), rather than individual protocells, evolved under the constraints of molecular complementarity. Composomes evolved into the hyperstructures of modern bacteria. We extend the ecosystems-first approach to explain the origin of eukaryotic cells through the integration of mixed populations of bacteria. We suggest that mutualism and symbiosis resulted in cellular mergers entailing the loss of redundant hyperstructures, the uncoupling of transcription and translation, and the emergence of introns and multiple chromosomes. (Abstract 2611)

In order to understand our argument, it is necessary to think of evolution not as the elaboration of individual traits, but as selection for more and more efficient ecologies. Thus, we propose that eukaryotic species did not evolve from elaboration or complexification of individual prokaryotic species, but rather that individual eukaryotic species evolved by integration and simplification from communities of diverse prokaryotes. (2612)

Palmer, Jeffrey, organizer. Symbiosis as an Evolutionary Driver: Mergers of Cells and Genomes. http://www.aaas.org/meetings/2009/program/lectures/topical.shtml.. From this web page, click on Program Planner, then on Browse, next on the Category. At the 2009 American Association for the Advancement of Science meeting in Chicago, a session under “Biological Science and Genomics” with this notable abstract. Palmer of Indiana University, along with Dalhousie University’s John Archibald, and Nancy Moran of the University of Arizona will speak. A broader AAAS overall program than in past years, it is worth searching among the many topics.

The endosymbiotic “hypothesis” for the origin of plastids and mitochondria from once free-living cyanobacteria and proteobacteria is now textbook “fact,” yet many fascinating aspects of the subsequent evolution of these organelles and their genomes have only recently been revealed thanks to the power of genomics. These include the following: mitochondrial genomes have repeatedly been lost during eukaryotic evolution, with the resulting organelles barely recognizable as endosymbionts; secondary, tertiary, etc., eukaryotic-eukaryotic symbioses have spread plastids and photosynthesis to the far corners of the eukaryotic world, leading to Russian Doll cells containing genes derived from up to a dozen different eukaryotic and endosymbiont genomes; the contribution of the original bacterial genome to the proteome of many mitochondria is remarkably dwarfed by that of the host eukaryotic genome; much has been learned about mechanisms of the functional transfer of organelle genes to the nucleus, as well as its remarkably punctuated tempo and pattern; and plant mitochondrial genes (and sometimes whole genomes) are transferred horizontally surprisingly often. Scientists are also only beginning to appreciate the ubiquity and metabolic diversity of latter-day symbioses of bacteria among eukaryotes. Bacterial symbionts of insects are best studied and display a remarkable range of genome sizes and gene repertoires, with some quite possibly having “crossed the line” from endosymbionts to organelles.

Pereira, Luisa, et al. A Symbiogenic Way in the Origin of Life. Seckbach, Joseph, ed. Genesis - In the Beginning. Dordrecht: Springer, 2012. With coauthors Telma Rodrigues and Francisco Carrapico, University of Lisbon biologists contribute an extensive chapter which makes a good case for the presence and inclusion of an evolutionary propensity for such “reticulated,” cooperative mutuality. Within the book’s Astrobiology theme, decades of symbiotic research and confirmation augur for the recognition of such a prior, creative force to Darwinian competition and selection alone. Indeed it is noted that Darwin actually noted this by his use of the term “concurrency” for these effects. As the quotes convey, such witness of a “universal symbiogenesis” (search Gontier) via a complementarity of agental and relational phases from pre-life forward quite appears as another result of nature’s innate self-organization.

The symbiogenic concept allows an innovative approach to the origin and evolution of life, with applicability to life’s initial stages, and capable of being a fundamental rule in life’s establishment and development on Earth and elsewhere. We suggest a naturalistic explanation for the origin of life, through the evolution of complex and adaptative systems, with synergistic, cooperative and symbiogenic mechanisms, guiding chemical evolution through its constraints. (729) We believe this definition allows different phenomena to be regarded as symbiogenic, and that universal symbiogenesis provides us with a general analytical tool for the immense interactions among different entities, namely the prebiotic and biotic entities. The symbiogenesis concept, through universal symbiogenesis, can be applied to the prebiotic evolutive context, beyond the biotic one, as a new paradigm shift in evolution. The science of complexity defies the selectionist hegemony, by arguing that such a long-term trend toward increasing complexity suggests the presence of additional mechanism(s). (729)

We believe that cooperative and synergistic processes were responsible, using terrestrial and extraterrestrial materials, for the creation of a large prebiotic pool, closely related to geochemical contexts, and intense interactions within. Most likely, a series of synergistic and cooperative effects produced a wide source of creativity, and functional advantages that pushed the emergence of complex and functionally integrated biological systems, through the evolution of self-organization and autocatalysis. It was only after this biochemical evolution of structures, which produced the informational capabilities necessary to self-replication, that the Darwinian mechanisms could arise. (739)

Pradeu, Thomas. A Mixed Self: The Role of Symbiosis in Development. Biological Theory. 6/1, 2012. In a thematic issue on how organisms develop, a Paris-Sorbonne University philosopher of biology argues for an expanded view of individuals. Rather than a closed system, creatures abide in and horizontally interact with environments. Mutualities, often bacterial, expand such selves into such reciprocal communities.

Since the 1950s, the common view of development has been internalist: development is seen as the result of the unfolding of potentialities already present in the egg cell. In this article, I show that this view is incorrect because of the crucial influence of the environment on development. I focus on a fascinating example, that of the role played by symbioses in development, especially bacterial symbioses, a phenomenon found in virtually all organisms (plants, invertebrates, and vertebrates). I claim that we must consequently modify our conception of the boundaries of the developing entity, and I show how immunology can help us in accomplishing this task. I conclude that the developing entity encompasses many elements traditionally seen as “foreign,” while I reject the idea that there is no possible distinction between the organism and its environment. (Abstract, 80)

Prosdocimi, Francisco, et al. The Theory of Chemical Symbiosis: A Margulian View for the Emergence of Biological Systems. Acta Biotheoretica. 69/1, 2021. We note this entry by Universidade Federal do Rio de Janeiro, Universidad Nacional Autónoma de México and Universidade Federal do Rio de Janeiro, Universidade Federal da Paraíba, Brazil biochemists as an example of how symbiotic phenomena are being found in increasingly widespread areas as in this case of life’s origins. As the title cites, some ten years after Lynn Margulis’ passing, there is strong effort is going forth to give prime credit to her four decades of study, explanation and defense.

The theory of chemical symbiosis (TCS) suggests that biological systems started with the collaboration of two polymeric molecules existing in early Earth: nucleic acids and peptides. Chemical symbiosis emerged when RNA-like nucleic acid polymers happened to fold into 3D structures capable to bind amino acids together, forming a proto peptidyl-transferase center. TCS suggests that there is no chicken-and-egg problem into the emergence of biological systems as RNAs and peptides were of equal importance to the origin of life. Life has initially emerged when these two macromolecules started to interact in molecular symbiosis. Mutualism is the strongest force in biology, capable to create novelties by emergent principles; on which the whole is bigger than the sum of the parts. (Abstract excerpt)

Rivera, Marla and James Lake. The Ring of Life Provides Evidence for a Genome Fusion Origin of Eukaryotes. Nature. 431/152, 2005. In the beginning, gene interchanges between microbes was a major driver of more complex organic assemblies. But the shape of life’s evolutionary profusion depends on what criteria it is based on. If per genomes alone, then a cladistic tree, bush, coral or “ring” accrues. When an ascent of intelligence is added a more directional path is revealed.

Genomes hold within them the record of the evolution of life on Earth. But genome fusions and horizontal gene transfer seem to have obscured sufficiently the gene sequence record such that it is difficult to reconstruct the phylogenetic tree of life. Here we determine the general outline of the tree using complete genome data from representative prokaryotes and eukaryotes and a new genome analysis method that makes it possible to reconstruct ancient genome fusions and phylogenetic trees. Our analyses indicate that the eukaryotic genome resulted from a fusion of two diverse prokaryotic genomes, and therefore at the deepest levels linking prokaryotes and eukaryotes, the tree of life is actually a ring of life. One fusion partner branches from deep within an ancient photosynthetic clade, and the other is related to the archaeal prokaryotes. The eubacterial organism is either a proteobacterium, or a member of a larger photosynthetic clade that includes the Cyanobacteria and the proteobacteria. (Abstract 152)

Rives, Alexander and Timothy Galitski. Modular Organization of Cellular Networks. Proceedings of the National Academy of Sciences. 100/1128, 2003. Protein complexes are found to form functional modules contained in universal scale-free networks with a nonrandom power-law distribution. (This is also how the brain organizes itself.)

Driven by the acquisition of whole-genome-scale data sets from complex biological systems, our conception of biomolecular organization is evolving from metabolic and signaling pathways to networks of evolutionarily conserved modules. (1128)

Rizzotti, Martino. Early Evolution. Basel: Birkhauser, 2000. An account of the course of symbiotic complexification from the prokaryotics to eukarotes to multicellularity.

Robinson, Carol, et al. The Molecular Sociology of the Cell. Nature. 450/973, 2007. By employing novel experimental techniques such as mass spectrometry of protein complexes, an internal neighborhood of ‘functional modules’ can now be discerned. The article is from a special section on Proteins to Proteomes (similar to genome, all the proteins of an organism), which also contains Dynamic Personalities of Proteins, by Katherine Henzler-Wildman and Dorothee Kern.

Rosenberg, Eugene and Ilana Zilber-Rosenberg. Microbes Drive Evolution of Animals and Plants: The Hologenome Concept. mBio. 7/2, 2016. In this American Society for Microbiology online journal, the Tel Aviv University microbiologists who first conceived this term (search) continue to quantify and explain its presence within and across fauna and flora. See also Introduction to the Hologenome Special Series by Margaret McFall-Ngai and Speciation by Symbiosis by Dylan Shropshire and Seth Bordenstein in this issue.

The hologenome concept of evolution postulates that the holobiont (host plus symbionts) with its hologenome (host genome plus microbiome) is a level of selection in evolution. Multicellular organisms can no longer be considered individuals by the classical definitions of the term. Every natural animal and plant is a holobiont consisting of the host and diverse symbiotic microbes and viruses. Microbial symbionts can be transmitted from parent to offspring by a variety of methods, including via cytoplasmic inheritance, coprophagy, direct contact during and after birth, and the environment. A large number of studies have demonstrated that these symbionts contribute to the anatomy, physiology, development, innate and adaptive immunity, and behavior and finally also to genetic variation and to the origin and evolution of species. Acquisition of microbes and microbial genes is a powerful mechanism for driving the evolution of complexity. Evolution proceeds both via cooperation and competition, working in parallel. (Abstract)

Roughgarden, Joan, et al. Holobiont as Units of Selection and a Model of Their Population Dynamics and Evolution. Biological Theory. Online September, 2017. In 1991 the microbiologist Lynn Margulis (1938-2011) proposed this title term for organisms in truth as symbiotic assemblages. The concept which has lately gained import and usage is given wide exposition by Joan Roughgarden, University of Hawaii, Scott Gilbert, Swarthmore College, Eugene and Ilana Zilber-Rosenberg, Tel-Aviv University, and Elisabeth Lloyd, Indiana University. Herein holobionts are seen to possess integrated anatomical, physiological, developmental, interactive, genomic qualities and functions within an overall viability. A January 2018 MIT Press book Landscapes of Collectivity in the Life Sciences, edited by Snait Gissis, et al will provide a major statement. And as proof of the actual utility of this holobiont/genome perception, it is used in Our Gut Microbiome: The Evolving Inner Self by Paraq Kundu, et al in the journal Cell (171/7, 2017) without even citing these origins.

Holobionts, consisting of a host and diverse microbial symbionts, function as distinct biological entities anatomically, metabolically, immunologically, and developmentally. Symbionts can be transmitted from parent to offspring by a variety of vertical and horizontal methods. Holobionts can be considered levels of selection in evolution because they are well-defined interactors, replicators/reproducers, and manifestors of adaptation. An initial mathematical model is presented to help understand how holobionts evolve. The model offered combines the processes of horizontal symbiont transfer, within-host symbiont proliferation, vertical symbiont transmission, and holobiont selection. The model offers equations for the population dynamics and evolution of holobionts whose hologenomes differ in gene copy number, not in allelic or loci identity. The model may readily be extended to include variation among holobionts in the gene identities of both symbionts and host. (Abstract)

Ryan, Frank. Darwin’s Blind Spot: Evolution Beyond Natural Selection. Boston: Houghton Mifflin, 2002. A British physician extols the unappreciated presence and force of symbiotic assembly in the advancement of life.

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