Lynn Margulis

Biological Modulation of the Earth's Atmosphere

Abstract We review the evidence that the Earths atmosphere is regulated by life on the surface so that the probability of growth of the entire biosphere is maximized. Acidity, gas composition including oxygen level, and ambient temperature are enormously important determinants for the distribution of life. We recognize that the earths atmosphere deviates greatly from that of the other terrestrial planets in particular with respect to acidity, composition, redox potential and temperature history as predicted from solar luminosity. These deviations from predicted steady state conditions have apparently persisted over millions of years. We explore the concept that these anomalies are evidence for a complex planet-wide homeostasis that is the product of natural selection. Possible homeostatic mechanisms that may be further investigated by both theoretical and experimental methods are suggested.

Protist classification and the kingdoms of organisms

Traditional classification imposed a division into plant-like and animal-like forms on the unicellular eukaryotes, or protists; in a current view the protists are a diverse assemblage of plant-, animal- and fungus-like groups. Classification of these into phyla is difficult because of their relatively simple structure and limited geological record, but study of ultrastructure and other characteristics is providing new insight on protist classification. Possible classifications are discussed, and a summary classification of the living world into kingdoms (Monera, Protista, Fungi, Animalia, Plantae) and phyla is suggested. This classification also suggests groupings of phyla into superphyla and form-superphyla, and a broadened kingdom Protista (including green algae, oomycotes and slime molds but excluding red and brown algae). The classification thus seeks to offer a compromise between the protist and protoctist kingdoms of Whittaker and Margulis and to combine a full listing of phyla with grouping of these for synoptic treatment.

Colchicine-Sensitive Microtubules

Publisher Summary Colchicine and several other compounds are fine tools for analyzing the assembly of a microtubule protein into tubules. Microtubules underlie the development of asymmetric cell shapes. Slow morphogenetic movements involving microtubule polymerization tend to be colchicine sensitive. Microtubules may be considered cellular skeletons, especially with respect to the development of a new form, but they may also be intimately involved in other complex functions of eukaryotic cells. The assembly of a microtubule protein into mitotic spindle microtubules may account directly for the generation of force in mitosis. In addition, conformational changes in microtubule protein may account for the chemosensitivity of the nervous system of higher animals. The interactions of tubulin proteins with small molecules explain the processes of touch, hearing, olfaction, chemotaxis, and generation of action potentials.

Methanogenesis, fires and the regulation of atmospheric oxygen.

Abstract The Gaia hypothesis states that the composition, oxidation-reduction potential and the temperature of the Earths lower atmosphere are modulated by and for the biota living on the surface (Lovelock, 1972; Margulis and Lovelock, 1974). A corollary is that atmospheric oxygen is presently regulated at about 21% for the dominant life forms today: vascular plants and metazoa. We suggest that the enormous annual production of methane (of the order of 10 14 mol) is directly related to the short term modulation of oxygen concentration. Atmospheric oxygen results from the burial of reduced carbon; methanogenesis and subsequent atmospheric oxidation of methane prevents that burial. We also present experimental work on the probability of ignition of vegetation as a function of increasing oxygen concentration (Watson, 1978). Both the experiments and consideration of the fossil record lead us to conclude that oxygen has been regulated by methane (and perhaps by N 2 O and others) at about 10–25% for very long periods relative to the atmospheric residence times of these reactive gases.

On the experimental silicification of microorganisms II. On the time of appearance of eukaryotic organisms in the fossil record

Abstract On the basis of ultrastructural, biochemical and genetic studies, bacteria and blue green algae (Kingdom Monera, all prokaryotes) differ unambiguously from the eukaryotic organisms (Fungi, plants sensu stricto ) and protists or protoctists, (Copeland, 1956). The gap between eukaryotes and prokaryotes is recognized as the most profound evolutionary discontinuity in the living world. This gap is reflected in the fossil record. Fossil remains of Archaean and Proterozoic Aeons primarily consist of prokaryotes and the Phanerozoic is overwhelmingly characterized by fossils of the megascopic eukaryotic groups, both metazoa and metaphyta. Based on the morphological interpretation of microscopic objects structurally preserved in Precambrian cherts, the time of appearance of remains of eukaryotic organisms in the fossil record has been claimed to be as early as 2.7 · 10 9 years ago, (Kaźmierczak, 1976). Others suggest chronologies varying between 1.7 to 1.3 · 10 9 (Schopf et al., 1973) or a time approaching 1.3 · 10 9 years (Cloud, 1974). There is general agreement that many of the Ediacaran faunas, which have been dated at about 680 m.y. are fossils of megascopic soft-bodied invertebrate animals. Since all invertebrates are eukaryotic, the ca. 680 m.y. date for deposition of these animal assemblages may represent the earliest appearance of eukaryotic organisms. But the question remains as to whether there is definitive evidence for eukaryotic cells before this “benchmark” of the late Precambrian. An excellent discussion of this particular problem as especially relating to acritarchs extending from rocks of Upper Riphean through Vendian and into the basal Cambrian is presented in recent studies by Vidal (1974, 1976) in Late Precambrian microfossils from the Visingso rocks of southern Sweden. Previous work on the laboratory silicification of wood and algal mat communities (Leo and Barghoorn, 1976) suggested that further analysis of “artificial fossils” might be of aid in the interpretation of fossil morphology toward the ultimate solution of this problem. Thus the procedure developed by one of us (ESB) for laboratory wood silicification was adapted to various smaller objects. By successive immersions of wet cellular aggregates, colonies of various organisms and abiotic organic microspheres in tetraethyl orthosilicate, silicified cells and structures are produced which bear an interesting resemblance to ancient chert-embedded microfossils. Our observation of these microorganisms and proteinoid microspheres silicified in the laboratory as well as of degrading microorganisms, both eukaryotic and prokaryotic, have led us to conclude that many, if not all, of the criteria for assessing fossil eukaryotic microorganisms are subject to serious criticism in interpretation. We studied a large variety of prokaryotic algae, some eukaryotic algae, fungi, protozoa, and abiotic organic microspheres stable at essentially neutral pH. In some cases, degradation and/or silicification systematically altered both size and appearances of microorganisms. By the use of monoalgal cultures of blue-green algae, features resembling nuclei, chloroplasts, tetrads, pyrenoids, and large cell size may be simulated. In many cases individual members of these cultures show so much variation that they may be mistaken as belonging to more than one species. The size ranges for silicified prokaryotic and eukaryotic algae overlap. Several prokaryotes routinely yielded spherical or filamentous structures that resembled large cells. Because of genuine large sizes (e.g., Prochloron ), shrinkage, systematic alteration or congregation of unicells to form other structures we find sizes to be of very limited use in determining whether an organism of simple morphology was prokaryotic or eukaryotic. Although some “prebiotic proteinoid microspheres” (of Fox and Harada, 1960) are impossible to silicify with our laboratory methods, those stable at neutral pH (Hsu and Fox, 1976) formed spherical objects that morphologically resemble silicified algae or fungal spores. Many had internal structure. We conclude that even careful morphometric studies of fossil microorganisms are subject to many sources of misinterpretation. Even though it is a logical deduction that eukaryotic microorganisms evolved before Ediacaran time there is no compelling evidence for fossil eukaryotes prior to the late Precambrian metazoans.

The last eukaryotic common ancestor (LECA): Acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon

We develop a symbiogenetic concept of the origin of eukaryotic intracellular motility systems from anaerobic but aerotolerant spirochetes in sulfide-rich environments. The last eukaryotic common ancestors (LECAs) have extant archaeprotist descendants: motile nucleated cells with Embden-Meyerhof glycolysis and substrate-level phosphorylation that lack the α-proteobacterial symbiont that became the mitochondrion. Swimming and regulated O2-tolerance via sulfide oxidation already had been acquired by sulfidogenic wall-less archaebacteria (thermoplasmas) after aerotolerant cytoplasmic-tubule-containing spirochetes (eubacteria) attached to them. Increasing stability of sulfide-oxidizing/sulfur-reducing consortia analogous to extant sulfur syntrophies (Thiodendron) led to fusion. The eubacteria–archaebacteria symbiosis became permanent as the nucleus evolved by prokaryotic recombination with membrane hypertrophy, analogous to Gemmata obscuriglobus and other δ-proteobacteria with membrane-bounded nucleoids. Histone-coated DNA, protein-synthetic RNAs, amino-acylating, and other enzymes were contributed by the sulfidogen whereas most intracellular motility derives from the spirochete. From this redox syntrophy in anoxic and microoxic Proterozoic habitats LECA evolved. The nucleus originated by recombination of eu- and archaebacterial DNA that remained attached to eubacterial motility structures and became the microtubular cytoskeleton, including the mitotic apparatus. Direct LECA descendants include free-living archaeprotists in anoxic environments: archamoebae, metamonads, parabasalids, and some mammalian symbionts with mitosomes. LECA later acquired the fully aerobic Krebs cycle-oxidative phosphorylation-mitochondrial metabolism by integration of the protomitochondrion, a third α-proteobacterial symbiont from which the ancestors to most protoctists, all fungi, plants, and animals evolved. Secondarily anaerobic eukaryotes descended from LECA after integration of this oxygen-respiring eubacterium. Explanatory power and experimental predictions for molecular biology of the LECA concept are stated.

Mitotic arrest by Melatonin

Abstract We are testing the hypothesis that migration of the newly formed mouth (i.e., oral membranellar band) in stentor is homologous to mitotic chromosomal movement and that both types of movement within single cells depend directly on microtubule elongation. The following compounds synchronously delay the migration of the oral membranellar band as an exponential function of concentration: Colcemid, podophyllotoxin, β-peltatin and vinblastine. Delay for these compounds can be described by the equation, y = kx n , where y is delay in hours and x is concentration of mitotic spindle inhibitor in moles/l. We discovered that the animal pineal gland hormone, melatonin (5-methoxy n -acetyl tryptamine), also specifically and reproducibly delays oral band regeneration according to an equation of this form. Thus we predicted that melatonin would arrest mitosis. We report here a colchicine-type disruption of the mitotic apparatus in onion root tips by melatonin. Two closely related tryptamine derivatives, n -acetyl serotonin and serotonin were inactive in both the stentor and onion assays: they neither delayed band migration in stentor as an exponential function nor induced mitotic arrest in onion.

The evolutionary transition from RNA to DNA in early cells

SummaryThe evolution of genetic material can be divided into at least three major phases: first, genomes of “nucleic acid-like” molecules; secondly, genomes of RNA; and finally, double-stranded DNA genomes such as those present in all contemporary cells. Using properties of nucleic acid molecules, we attempt to explain the evolutionary transition from RNA alone as a cellular informational macromolecule prior to the evolution of cell systems based on double-stranded DNA. The idea that ribonucleic acid-based cellular genomes preceded DNA is based on the following: (1) protein synthesis can occur in the absence of DNA but not of RNA; (2) RNA molecules have some catalytic properties; (3) the ubiquity of purine and pyridine nucleotide coenzymes as well as other similar ribonucleotide cofactors in metabolic pathways; and (4) the fact that the biosynthesis of deoxyribonucleotides always proceeds via the enzymatic reduction of ribonucleotides.The “RNA prior to DNA” hypothesis can be further developed by understanding the selective pressures that led to the biosynthesis of deoxyribose, thymine, and proofreading DNA polymerases. Taken together these observations suggest to us that DNA was selected as an informational molecule in cells to stabilize earlier RNA-protein replicating systems. These arguments include the facts that (1) the 2′-deoxy-containing phosphodiester backbone is more stable in aqueous conditions and in the presence of transition metal ions (such as Zn2+) than its ribo-equivalents; (2) the absence of proofreading activity in RNA polymerases leads to a higher rate of mutation in RNA genomes relative to DNA; (3) information in RNA degrades because of the tendency of cytosine to deaminate to uracil and the lack of a correcting enzyme; and (4) UV irradiation produces a larger number of photochemical changes in RNA molecules relative to double-stranded DNA. The absence of atmospheric UV attenuation during the early Earth environment (Hadean and early Archean) would have imposed an intense selection pressure favoring duplex DNA over other genetic information storage systems.If RNA preceded DNA as a reservior of cellular genetic information, then an RNA-replicating oligopeptide must have been one of the earliest protoenzymes from which RNA polymerase presumably evolved. We conclude that RNA polymerases are among the oldest classes of enzymes.

The Microbial Community in the Layered Sediments at Laguna Figueroa, Baja California, Mexico: Does it Have Precambrian Analogues?

Abstract In the hypersaline lagoon at Laguna Figueroa vertically stratified diverse communities of microorganisms thrive. The modern sediments of Baja California at Laguna Figueroa contain cyanobacterial communities and sedimentary structures produced by these blue greens that have already been studied by Horodyski and his colleagues. This paper provides an introduction to the complex microbial communities, primarily those that underlie the laminated Microcoleus mats. They are composed of anaerobic photosynthetic and heterotrophic bacteria. The following genera of cyanobacteria at least are components of these mat communities: Lyngbya, Microcoleus, Entophysalis, Phormidium, Pseudoanabaena, Anabaena and Schizothrix. Among the photosynthetic bacteria several species of Thiocapsa-like microbes formed major surface components of certain mats and scums; rhodospirilli, rhodopseudomonads, chromatis and others were seen. The following nonphotosynthetic bacteria were identified: Nocardia sp., three types of spirilli, two types of Spirochaeta sp., two types of Desulfovibria sp., a new strain of red Beneckea and four distinctive unidentified coccoid and filamentous bacteria. Reasons are given for believing several of the species are new to science and that the microbial diversity is far greater than the approximately twenty species reported here. Eukaryotes are extremely rare. Only one species of animal, a herpachtechoid copepod, was ever seen in the 8-km long microbial communities of the hypersaline basin. Dunaliella salina, a chlorophyte and Aspergillus sydowi, an ascomycetous fungus were the only eukaryotes that were observed to be regular components of mat communities. Ciliates, amoebae (including a chrysarchnion-like microbe) and diatom tests, mostly empty, were the only other eukaryotes observed. Attempts to enrich for eukaryotic microorganisms were not successful whereas attempts to enrich for bacteria, especially anaerobes led to such a profusion of forms that to continue detailed study of them was beyond our means. Unidentified small rods and cocci constituted the largest fraction of individuals in the subsurface community. The microbes isolated from mats are adapted for alternating dry and wet conditions as well as high concentrations of salt and low concentrations of oxygen.

Evolutionary Criteria in Thallophytes: A Radical Alternative

The classical assumptions, upon which all previous phylogenies for the lower plants (Thallophytes) have been based, are claimed to be erroneous. An alternative view, that the eukaryotic cell arose in the late Precambrian from prokaryotic ancestors by a specific series of symbioses, is referred to here. Mutually consistent phylogenies, one for the prokaryotes, another for the lower eukaryotes, can be constructed on the basis of the symbiotic theory. The resulting prokaryote phylogeny is presented here; it is claimed to be more consistent with cytological data, measured DNA base ratios, and the fossil record than the several classical partial phylogenies for Thallophytes recently published.