V. Life's Corporeal Evolution Develops, Encodes and Organizes Itself: An Earthtwinian Genesis Synthesis

3. Cellular Self-Organization and Holobiont Symbiogenesis

Rackaityte, Elze and Susan Lynch. The human microbiome in the 21st century. Nature Communications. 11/5256, 2020. A UC San Francisco biochemist and a gastroenterologist enter an introductory survey of growing realizations that our whole selves are actually multitudinous microbial ecosystems.

The human body supports a thriving diversity of microbes which comprise a dynamic, ancillary, functional system that synergistically develops in lock-step with physiological development of its host. The human microbiome field has transitioned from cataloging this rich diversity to dissecting molecular mechanisms by which microbiomes influence human health. Early life microbiome development trains immune function. Thus, vertically, horizontally, and environmentally acquired microbes and their metabolites have the potential to shape developmental trajectories with life-long implications for health. (Abstract)

Richards, Thomas and Nancy Moran. Symbiosis: In search of a deeper understanding. PloS Biology. April, 2024. Oxford University and UT Texas integrative biologists introduce eight articles which are meant as a belated admission of nature’s pervasive reciprocal interrelations between all manner of cellular embodiments, metabolic processes and environmental viability. This obvious feature can no longer be ignored for it has a primary evolutionary and organismic significance. Papers include What choanoflagellates can teach us about symbiosis by Arielle Woznica, Linking cell biology and ecology to understand coral symbiosis evolution by Niels Dingemanse and Annika Guse, Modeling endosymbioses by Lucas Santana Souza, et al, and Fungal holobionts as blueprints for synthetic endosymbiotic systems by Laila Partida-Martínez. But they often seem begrudged, with constant referrals to “mechanistic” reasons, along with not one mention of Lynn Margulis (search)who studied and advocated symbiosis since 1970.

The mechanistic biology that underpins symbiotic outcomes is fascinating. It is also where this field’s most interesting future lies. How do complex multifaceted symbiotic interactions emerge? How is partner specificity enacted? How is stability maintained under strong evolutionary MORE imperative towards exploitation and, therefore, interaction collapse? This collection demonstrates how the field is shifting to a growing focus on symbiotic interactions. By combining mechanistic and genetic understanding with evolutionary analysis, we can gain a direct view of how symbioses emerge. Only when we have this view for a range of systems can we look for unifying themes, if they even exist. (Abstract)

Symbiosis across the tree of life. Symbiosis research has become a holistic and pervasive field with a mature theoretical basis. Extraordinary diversity in symbiotic relationships exists across the tree of life. The aim of this special collection is to showcase symbiotic relationships across the tree of life, exploring their evolutionary basis and underlying mechanisms.

Once we have a deeper understanding of microbial endosymbionts in fungi, we will be able to design symbiotic systems that synergize the capabilities of fungi, bacteria, and viruses. These synthetic fungal holobionts could help us improve our crops to face climate change; restore eroded or contaminated soils; produce high-valued chemicals, enzymes, and other biomolecules and biomaterials; and increase the recycling of organic matter and plastics. (Laila P-M)

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. Holobiont Evolution: Population Theory for the Hologenome. American Naturalist. April, 2023. The University of Hawaii wise-wuman bioecologist posts a latest, thorough appreciation of the actual presence of life’s integrative cell and organism reciprocities. A detailed Abstract lists the many ways that this integral quality manifests and vivifies itself.

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.

Ryan, Frank. Genomic Creativity and Natural Selection. Biological Journal of the Linnean Society. 88/4, 2006. An expansion on his 2002 Darwin’s Blind Spot that cites, as the quote notes, an array of genetic and metabolic activities are at work prior to selection alone.

In the early 1930s, the synthesis of Darwinian natural selection, mutation, and Mendelian genetics gave rise to the paradigm of 'modern Darwinism', also known as 'neo-Darwinism'. But increasing knowledge of other mechanisms, including endosymbiosis, genetic and genomic duplication, polyploidy, hybridization, epigenetics, horizontal gene transfer in prokaryotes, and the modern synthesis of embryonic development and evolution, has widened our horizons to a diversity of possibilities for change. All of these can be gathered under the umbrella concept of 'genomic creativity', which, in partnership with natural selection, affords a more comprehensive modern explanation of evolution. (655)

Sagan, Dorion. From Empedocles to Symbiogenesis: Lynn Margulis’s Revolutionary Influence on Evolutionary Biology. Biosystems. June, 2021. We cite this latest essay as a succinct record of her valient endeavor to break out of old male fixation into a vital sense of an animate procreation graced by a universal principle of positive, reciprocal conciliations between all phases of organic entities. Yet we have a world tearing itself apart due to violent oppositions, which is in desperate need for such a unifying scientific vision. I have heard and met Lynn in Amherst, in my opinion she could merit being the one woman who could rise to the status of a Newton or Darwin.

As a primary expositor of the work of Lynn Margulis collaborating with her over thirty years on over thirty books and forty articles, scientific and popular, I attempt here to summarize her unique and lasting influence on evolutionary biology. Describing life on Earth as the multi-billion-year evolution of microbial communities, from prokaryotes maintaining Earth's atmosphere away from thermodynamic equilibrium to all eukaryotes as polygenomic beings, Margulis's interdisciplinary work has deeply influenced multiple fields including systematics, theories of the evolution of metabolism, paleobiology, and biogeochemistry. Overturning the neo-Darwinist narrative that speciation almost always occurs by the gradual accumulation of random mutations, Margulis's work revives a discarded philosophical speculation of the pre-Socratic Empedocles, who suggested that Earth's early beings both merged and differentially reproduced. Margulis's curiosity-driven science, collaborative work ethic, status as a woman, embrace of novelty, philosophical stance, current status of her theories, and the proposal for a new science of symbiogenetics are among the topics examined. (Abstract excerpt)

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