ArticlePDF Available

Osmotrophy in fossil protoctists and early animals

Authors:
... 565Ma;Fig. 6a-c), would also seem to burst the bubble on the idea of predator-less Ediacaran ocean floors and the "Garden of Ediacara" (McMenamin, 1993). ...
... Osmotrophy, the heterotrophic uptake of dissolved organic molecules across cell membranes, has been proposed as an alternative feeding mode in some Ediacaran macrobionts (McMenamin, 1993;Laflamme et al., 2009). This process can be viewed as type of partial saprotrophy where, rather than the organism excreting enzymes for external digestion and then absorbing the resulting products (dissolved organic matter, or DOM) within cells (as effected by fungi and bacteria, or the gut of animals), only absorption takes place. ...
Article
Full-text available
The earliest record of animal life come s from the Ediacaran of Newfoundland , including dm scale fossil organisms , most of which are inferred to have be en epibenthic immotile eumetazoans. This work introduces the palaeobiology of the major fossil groups in the Newfoundland assemblages including strange fractal-like taxa and addresses some of biogeochemical challenges such as sulfide buildup that could most easily have been overcome by symbiogenesis. Specifically, the epibenthic reclining nature of some of the Ediacaran biota with their fractal-like high surface area lower surfaces-are considered to have been well designed for gaining nutriment from chemosynthetic, sulfur-oxidizing bacteria. This view constitutes a shift away from the view that most of the biota were anomalously large osmotrophs.
... The protoeukaryote was capable of phagocytosis and potentially also osmotrophy (Raven, 1997;Martin et al., 2003). If the protoeukaryote was capable of osmotrophy, this may have been retained in the genome (McMenamin, 1993;Raven, 1997). Alternatively, a phagotrophic protoeukaryote requires a mechanism for transporting metabolites across a semi-permeable food vacuole membrane, which may have been retained in the protoeukaryote genome and expressed in the cell membrane (Jones, 2000;Martin et al., 2003). ...
Thesis
Full-text available
Mussel aquaculture is a low carbon source of protein and the mussel aquaculture industry in Scotland aims to double production. Reliance upon wild spat collection means that the industry is currently ‘at the mercy’ of spatially and temporally variable supply, with only 40% of spat collection sites producing sufficient larvae. One solution to this issue is to develop a larval hatchery; however, the requirement by larvae for large quantities of live microalgae results in high costs, relative to the value of spat. In this study, three microalgal species: Tetraselmis suecica, Phaeodactylum tricornutum and Cyclotella cryptica were screened for mixotrophic or heterotrophic growth with glucose, glycerol or acetate. These strains had a shift in the fatty acid profile in favour of shorter chain, saturated fatty acids and an increased carbohydrate content, depending upon strain, carbon source and harvesting time. Isotopically labelled glucose and inorganic carbon indicated that there was an increased partitioning of inorganic derived carbon into total fatty acids (4.19 % dry weight compared to 2.13 %) in autotrophic cultures, alongside lipid membrane remodelling in T. suecica. Other cost reduction strategies were trialled including media optimisation, screening for growth of P. tricornutum with crude glycerol and quantifying changes in the nutrient removal from the media. Utilising the identified strains and culture conditions, these microalgae were successfully used as feed for mussel larvae, both as single species and mixed diets. These diets performed as well as an ‘industry standard reference’ diet in terms of larval growth and survival. Furthermore, optimisation of the mixotrophic diet to account for increasing larval size resulted in both maximum larval growth (174.35 µm) and total fatty acid content (5.84 % dry weight). First order modelling indicated that mixotrophic culture of microalgae may reduce the costs of microalgal culture for a larval hatchery. The ability to maximise cellular density and tailor the biochemical profiles of these mixotrophic algae to develop ‘designer’ feed has potential to expand the uses of microalgae to other aquaculture species and the biotechnology industry
... Unlike these living forms, however, rangeomorphs appear to lack tentacles, openings or any other feedingrelated features, even in specimens preserving detail on a scale of tens of micrometres (Narbonne, 2004). As such, it has been widely assumed that nutrient uptake took place on the outside of the organism, after the manner of osmotrophic bacteria or fungi (McMenamin, 1993;Laflamme et al. 2009;Sperling et al. 2011). Certainly the characteristic 'fractal' branching would have increased the proportion of exposed surface area on which this might have occurred, but it remains to be demonstrated that rangeomorphs could actually feed in this fashion (Liu et al. 2015). ...
Article
Full-text available
Ediacaran rangeomorphs were the first substantially macroscopic organisms to appear in the fossil record, but their underlying biology remains problematic. Although demonstrably heterotrophic, their current interpretation as osmotrophic consumers of dissolved organic carbon (DOC) is incompatible with the inertial (high Re ) and advective (high Pe ) fluid dynamics accompanying macroscopic length scales. The key to resolving rangeomorph feeding and physiology lies in their underlying construction. Taphonomic analysis of three-dimensionally preserved Charnia from the White Sea identifies the presence of large, originally water-filled compartments that served both as a hydrostatic exoskeleton and semi-isolated digestion chambers capable of processing recalcitrant substrates, most likely in conjunction with a resident microbiome. At the same time, the hydrodynamically exposed outer surface of macroscopic rangeomorphs would have dramatically enhanced both gas exchange and food delivery. A bag-like epithelium filled with transiently circulated seawater offers an exceptionally efficient means of constructing a simple, DOC-consuming, multicellular heterotroph. Such a body plan is broadly comparable to that of anthozoan cnidarians, minus such derived features as muscle, tentacles and a centralized mouth. Along with other early bag-like fossils, rangeomorphs can be reliably identified as total-group eumetazoans, potentially colonial stem-group cnidarians.
... Evidence for lower, submodern oxygen levels in the Ediacaran oceans, in tandem with observed decoupling between Ediacaran organic and carbonate carbon stable isotope records, led, more than a decade ago, to the hypothesis that the Ediacaran global ocean was characterized by a large, heterogeneous, and labile pool of dissolved organic carbon (DOC) (Rothman et al. 2003 This high marine DOC model, in turn, lent renewed credence to the long-standing (Seilacher 1984, McMenamin 1993 model that many Ediacara Biota macroorganisms were osmotrophic. In particular, investigators have inferred that many of the rangeomorph taxa that dominate the faunal diversity of the Avalon Assemblage sustained themselves by means of osmotrophy, on the basis of the high-DOC model, as well as their fractal morphology and the deeper water, sub-wave base environment characteristic of many Avalon-type deposits (Sperling et al. 2007, Laflamme & Narbonne 2008). ...
Article
Full-text available
The evolutionary trajectory of early complex life on Earth is interpreted largely from the fossils of the Precambrian soft-bodied Ediacara Biota, which appeared and evolved during a time of dynamic biogeochemical and environmental fluctuation in the global ocean. The Ediacara Biota is historically divided into three successive Assemblages—the Avalon, the White Sea, and the Nama—whichare marked by the appearance of novel biological traits and ecological strategies. In particular, the younger White Sea and Nama Assemblages record a “second wave” of ecological innovations, which included the development of not only uniquely Ediacaran body plans and ecologies, such as matground adaptations, but also the dual emergence of bilaterian-grade animals and Phanerozoic-style ecological innovations, including spatial heterogeneity, complex reproductive strategies, ecospace utilization, motility, and substrate competition. The late Ediacaran was an evolutionarily dynamic time characterized by strong environmental control over the distribution of taxa in time and space. Expected final online publication date for the Annual Review of Earth and Planetary Sciences Volume 45 is May 30, 2017. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Article
Full-text available
The Ediacaran biota were soft-bodied organisms, many with enigmatic phylogenetic placement and ecology, living in marine environments between 574 and 539 million years ago. Some studies hypothesize a metazoan affinity and aerobic metabolism for these taxa, whereas others propose a fundamentally separate taxonomic grouping and a reliance on chemoautotrophy. To distinguish between these hypotheses and test the redox-sensitivity of Ediacaran organisms, here we present a high-resolution local and global redox dataset from carbonates that contain in situ Ediacaran fossils from Siberia. Cerium anomalies are consistently >1, indicating that local environments, where a diverse Ediacaran assemblage is preserved in situ as nodules and carbonaceous compressions, were pervasively anoxic. Additionally, δ ²³⁸ U values match other terminal Ediacaran sections, indicating widespread marine euxinia. These data suggest that some Ediacaran biotas were tolerant of at least intermittent anoxia, and thus had the capacity for a facultatively anaerobic lifestyle. Alternatively, these soft-bodied Ediacara organisms may have colonized the seafloor during brief oxygenation events not recorded by redox proxy data. Broad temporal correlations between carbon, sulfur, and uranium isotopes further highlight the dynamic redox landscape of Ediacaran-Cambrian evolutionary events.
Chapter
A diverse fauna of Ediacarans from the Clemente Formation of northwestern Sonora, México, includes Pteridinium cf. P. simplex, a recumbent sand frond Beothukis cf. B. mistakensis, the kimberellomorph Kimberella cf. K. quadrata, the solzid kimberellomorph Zirabagtaria ovata n. gen. n. sp., the praecambridiid Palankiras palmeri n. gen. n. sp., Vendamonia truncata n. gen. n. sp., and the aculiferans Clementechiton sonorensis McMenamin and Fleury, 2016 and Korifogrammia clementensis n. gen. n. sp. The Clemente biota provides new data regarding the Ediacaran Cuticle Paradox, which holds that in spite of their apparent simplicity, the Ediacaran cuticle in fact hosted a highly complex morphogenetic field. In a corollary of Williston’s Law, this cuticle underwent successive simplification at the end of the Proterozoic.
Chapter
Why does the Proterozoic shelly fossil Qinella occur in a Cambrian limestone? Qinella’s unique shell morphology, thin walls separated by fluid–filled spaces (etch stop defense), served as an effective deterrent to Cambrian shell–boring predators. Family Cloudinidae was likely driven to extinction by first boring, and later crushing, predators. Qinella provides an excellent example of the predator–prey escalation that took place during the Early Cambrian.
Article
The purpose of this review is to draw attention to the contribution that Nama sediments and fossils have made, and potentially can make, to the ongoing debate about metazoan origins. Two important features of this debate concern the nature and systematic position of the late Proterozoic "Ediacaran" fauna as well as the reasons for the sudden appearance in the fossil record of representatives of almost all known animal phyla, during the Early-Middle Cambrian radiation. An additional vexing question is the reason for the apparent absence of preserved representatives of ancestral metazoan lineages in Proterozoic sediments, despite the fact that molecular evidence shows that such lineages had a long history, prior to Cambrian times. Nama fossils and their enclosing sediments have made crucial contributions to this debate and will surely continue to do so in the future.
Article
When each of the Avalon-, Ediacara-, and Nama-type fossil assemblages are tracked through geological time, there appear to be changes in species composition and diversity, almost synchronized between different sedimentary environments, allowing a subdivision of the late Ediacaran into the Redkinian, Belomorian and Kotlinian geological time Intervals. The Redkinian (580-559 Ma) is characterized by first appearance of both eumetazoan traces and macroscopic organisms (frondomorphs and vendobionts) in a form of Avalon-type communities in the inner shelf environment, whereas coeval Ediacara-type communities remained depauperate. The Belomorian (559-550 Ma) is marked by the advent of eumetazoan burrowing activity in the inner shelf, diversification of frondomorphs, migration of vendobionts from the inner shelf into higher energy environments, and appearance of tribrachiomorphs and bilateralomorphs. Ediacaran organisms formed distinctive ecological associations that coexisted in the low-energy inner shelf (Avalon-type communities), in the wave-and current-agitated shoreface (Ediacara-type communities), and in the high-energy distributary systems (Nama-type communities). The Kotlinian (550-540 Ma) witnessed an expansion of the burrowing activity into wave-and current-agitated shoreface, disappearance of vendobionts, tribrachiomorphs and bilateralomorphs in wave-and current-agitated shoreface, together with a drop in frondomorph diversity. High-energy distributary channel systems of prodeltas served as refugia for Nama-type communities that survived until the end of the Ediacaran and disappeared when the burrowing activity reached high-energy environments. This pattern is interpreted as an expression of ecosystem engineering by eumetazoans, with the Ediacaran organisms being progressively outcompeted by bilaterians.
Article
Up to the 1950s, the Precambrian was regarded as unrewardingly unfossiliferous, records of fossils being isolated, few in number and dubious. The change came with the discovery by Reg Sprigg of body fossils in latest Proterozoic sediments in South Australia. Although there had been descriptions of isolated fossils (now recognised as Ediacaran) from rocks of this age in the nineteenth century and at the start of the twentieth century, in Newfoundland and Namibia, respectively, the Ediacara finds stimulated researches and now, at the start of the twenty-first century, diversified fossil assemblages are known, all over the world, from the period 600–543 Ma, known formerly as the Vendian and now officially as the Ediacaran. In this account, a brief description of the history of these finds is given, followed by descriptions of the most important provinces [South Australia, Leicestershire, Namibia, Russia (Podolia, the White Sea Coast, Urals and Siberia), Newfoundland (Avalon Peninsula) and Northwest Canada]: then of 27 other known occurrences of this dominantly soft-bodied and perplexing fauna(?)–it seems certain that some, at least of the fossils, are animal fossils, although some, even the greater part, could be a unique form of life, not animals or plants (“Vendobionta”). These descriptions, derived in the course of a literature search lasting over a year, are followed by discussions of important special aspects: trace fossils; geochronology and correlation; geotectonics; glaciation (the “Snowball Earth” concept applied to the Varangian/Laplandian/Marinoan glaciation, which ushered in this last subdivision of the Proterozoic); the evidence for Ediacaran and other life forms existing in the Proterozoic prior to its last, Ediacaran, chronological subdivison; the Vendozoa concept. The last section consists of short summary of conclusions. This text essentially constitutes an objective record of what has been published to 2005 on the Ediacaran System.
Article
Full-text available
The oxidation of the Earth's crust and the increase in atmospheric oxygen early in Earth history have been linked to the accumulation of reduced carbon in sedimentary rocks. Trends in the carbon isotope composition of sedimentary organic carbon and carbonate show that during the Proterozoic aeon (2.5-0.54 Gyr ago) the organic carbon reservoir grew in size, relative to the carbonate reservoir. This increase, and the concomitant release of oxidizing power in the environment, occurred mostly during episodes of global rifting and orogeny.
Book
In this classic series-generating paleontology/geology book published by Columbia University Press, Mark and Dianna McMenamin explore the evolutionary and paleoecological questions associated with the Cambrian Explosion. This book both names and maps the initial paleogeographic reconstruction of the billion year old supercontinent Rodinia. The observations and interpretations in this book, particularly as regards the timing of the Cambrian Explosion, have stood the test of time. The issues identified herein as most important for understanding the Proterozoic-Cambrian transition, remain so today.
Article
Dickinsonia is reconstructed as a benthic polypoid of generally cnidarian design. The oral surface was without tentacles but contained a median oral slit that probably led through a pharynx into an enteron, which was divided into digestive diverticulae by radiating mesenteries; feeding may have been via ciliary tracts. The mesenteries and body wall contained a stiff form of mesogloea. There seems to be no need to postulate a novel constructional grade for this organism, bringing the concept of the Vendozoa into question. -Author
Article
A method is described for the rapid, precise determination of non-volatile dissolved organic carbon in seawater in concentrations between 0 and 2000 μM. The oxidation is carried out on a platinum catalyst at 680 °C under an oxygen atmosphere after the sample has been freed of inorganic carbon, and the concentration of the CO2 generated is measured with a non-dispersive IR gas analyzer. The determination can be carried out on board ship with a precision of ±2% using a sample volume of 200 μl. The results obtained using this method are of a much higher value than those obtained using persulfate oxidation methods. The molecular weight dependency of the results clearly indiates that the above discrepancy is caused by the low oxidation efficiency of the persulfate oxidation method against high-polymer organic matter dissolved in seawater. The results reveal that the concentration of dissolved organic carbon in surface water is about 300 μM and decreases with depth. An examination of molecular weight distribution indicates that the concentration of high-polymer organic carbon decreases rapidly from surface to deeper layers, with molecular weight ranging from 1.8 x 103 to 6 x 104 Dalton. It is noted that there is an inverse correlation between the concentration of dissolved organic carbon and apparent oxygen utilization (AOU). Frozen or acidified preservation of unfiltered samples does not give reliable results. An essential requirement for dissolved carbon analysis is membrane filtration just after sampling and real-time analysis on board. Because of the well-defined principle of the oxidation process, its reliability, the ease of sample handling and of the analytical procedure on board or in the land laboratory, and the consistency of the oceanographic parameters, this method is much more suitable for the analysis of marine dissolved organic carbon than the methods used previously.
Article
Homogenates of various lower land plants, aquatic angiosperms, and green algae were assayed for glycolate oxidase, a peroxisomal enzyme present in green leaves of higher plants, and for glycolate dehydrogenase, a functionally analogous enzyme characteristic of certain green algae. Green tissues of all lower land plants examined (including mosses, liverworts, ferns, and fern allies), as well as three freshwater aquatic angiosperms, contained an enzyme resembling glycolate oxidase, in that it oxidized l- but not d-lactate in addition to glycolate, and was insensitive to 2 mm cyanide. Many of the green algae (including Chlorella vulgaris, previously claimed to have glycolate oxidase) contained an enzyme resembling glycolate dehydrogenase, in that it oxidized d- but not l-lactate, and was inhibited by 2 mm cyanide. Other green algae had activity characteristic of glycolate oxidase and, accordingly, showed a substantial glycolate-dependent O(2) uptake. It is pointed out that this distribution pattern of glycolate oxidase and glycolate dehydrogenase among the green plants may have phylogenetic significance.Activities of catalase, a marker enzyme for peroxisomes, were also determined and were generally lower in the algae than in the land plants or aquatic angiosperms. Among the algae, however, there were no consistent correlations between levels of catalase and the type of enzyme which oxidized glycolate.