Osmotrophy in modular Ediacara organisms Marc Laflamme1, Shuhai Xiao, and Michał Kowalewski Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Edited by James W. Valentine, University of California, Berkeley, CA, and approved July 7, 2009 (received for review May 4, 2009) The Ediacara biota include macroscopic, morphologically complex fractal branching of rangeomorph modular units served to increase soft-bodied organisms that appear globally in the late Ediacaran the surface area to volume (SA/V) ratio to facilitate direct nutrient Period (575–542 Ma). The physiology, feeding strategies, and absorption (osmotrophy) of dissolved organic carbon (DOC) (8, functional morphology of the modular Ediacara organisms 11), which is presumed to have been abundant in Ediacaran deep (rangeomorphs and erniettomorphs) remain debated but are crit- oceans (12–14). ical for understanding their ecology and phylogeny. Their modular Osmotrophy in erniettomorphs and rangeomorphs requires construction triggered numerous hypotheses concerning their a high SA/V ratio to allow for rapid and effective transport likely feeding strategies, ranging from micro-to-macrophagus of nutrients directly through the integument. Today, true feeding to photoautotrophy to osmotrophy. Macrophagus feeding osmotrophy is restricted to microscopic bacteria with sizes in rangeomorphs and erniettomorphs is inconsistent with their lack typically Ͻ100 ␮m, although osmotrophic ‘‘giants,’’ such as of oral openings, and photoautotrophy in rangeomorphs is con- Thiomargarita and Epulopiscium (Table 1), have cell sizes up to tradicted by their habitats below the photic zone. Here, we 600 and 750 ␮m, respectively (15, 16). However, these prokary- combine theoretical models and empirical data to evaluate the otic giants are dwarfed by even the smallest erniettomorphs and feasibility of osmotrophy, which requires high surface area to rangeomorphs, raising the question of whether the inferred volume (SA/V) ratios, as a primary feeding strategy of rangeo- trophic models of these Ediacara fossils can be reconciled with morphs and erniettomorphs. Although exclusively osmotrophic their large body size. Thus, the goal of this study was to simulate feeding in modern ecosystems is restricted to microscopic bacteria, various morphological changes in the overall construction of this study suggests that (i) fractal branching of rangeomorph modular Ediacara organisms to test whether it is possible for modules resulted in SA/V ratios comparable to those observed in them to attain SA/V ratios on the same order as those seen in modern osmotrophic bacteria, and (ii) rangeomorphs, and partic- modern osmotroph bacteria. ularly erniettomorphs, could have achieved osmotrophic SA/V The use of strictly osmotrophic megabacteria as ecological ratios similar to bacteria, provided their bodies included metabol- analogues for rangeomorphs and erniettomorphs represents a ically inert material. Thus, specific morphological adaptations ob- conservative choice for comparative purposes. Should the hy- served in rangeomorphs and erniettomorphs may have repre- pothesis that rangeomorphs and erniettomorphs represent eu- sented strategies for overcoming physiological constraints that karyotic organisms be true, it is likely that these organisms would typically make osmotrophy prohibitive for macroscopic life forms. be able to supplement osmotrophy by endocytosis, thus reducing These results support the viability of osmotrophic feeding in the strict SA/V threshold suggested by giant bacteria. rangeomorphs and erniettomorphs, help explain their taphonomic Computer modeling of individual erniettomorph and rangeo- peculiarities, and point to the possible importance of earliest morph structural modules was performed to evaluate how SA/V macroorganisms for cycling dissolved organic carbon that may ratios would change with the addition, inflation, or vacuolization have been present in abundance during Ediacaran times. of individual modules. If the hypothesis that these organisms fed through direct diffusion is correct, the SA/V ratio should place erniettomorphs ͉ rangeomorphs ͉ Fractofusus ͉ Pteridinium a strong physiological constraint on the morphologies of erni- ettomorphs and rangeomorphs. he late Ediacaran Period marks the rapid diversification of Tglobally widespread macroscopic organisms: the soft-bodied Modeling Parameters and Justification and morphologically complex Ediacara biota. For the first time Modeling Erniettomorphs. We chose Pteridinium (Fig. 1 A and B) in Earth history, organisms constructed macroscopic body plans as a representative erniettomorph for modeling purposes be- allowing for moderate levels of ecological interactions and cause this organism is an optimal form to model, and there are competition for nutrients and substrate availability (1–3). The published specimen measurements for comparison with model- iconic, serially quilted erniettomorphs and fractally branched ing results (6). The modular units of Pteridinium are assumed to rangeomorphs (4) are the most poorly understood members of have been tubes with a square cross-section and assembled into the Ediacara biota because of their unique construction, un- three petaloids (vanes). Complete Pteridinium specimens are known from any Phanerozoic/modern groups (Fig. 1) (5). Erni- spindle-shaped, tapering at both ends and suggesting a bipolar ettomorphs are characterized by highly repeatable tubular units growth strategy (Fig. 1A). The earliest ontogenetic sequence of (6), whereas rangeomorphs consist of repeatedly branched module addition is difficult to interpret from Pteridinium, be- frondlets (7). Their body plans highlight a modularity in which cause even the smallest complete specimen consists of 37 individual units are assembled into complex, species-specific modules per petaloid (6). However, the comparison of numerous arrangements (4, 8, 9). However, the purpose of this growth arrangement has yet to be fully explored. The likely feeding strategy of these modular Ediacara organisms Author contributions: M.L., S.X., and M.K. designed research; M.L. performed research; M.K. contributed new reagents/analytic tools; M.L., S.X., and M.K. analyzed data; and M.L., has been a topic of considerable controversy. Interpretations varied S.X., and M.K. wrote the paper. from micro-to-macrophagus feeding, photoautotrophy, saprotro- The authors declare no conflict of interest. phy, and parasitism, to symbiosis (5, 10). However, a macrophagus This article is a PNAS Direct Submission. interpretation for erniettomorphs and rangeomorphs is contra- 1To whom correspondence should be sent at the present address: Department of Geology dicted by their lack of any macroscopic feeding structures (e.g., and Geophysics, Yale University, P.O. Box 208109, New Haven, CT 06520-8190. E-mail: tentacles, zooids, or oral openings), and rangeomorph photoaut- marc.lafl[email protected]. otrophy is inconsistent with their range of habitats, which extended This article contains supporting information online at www.pnas.org/cgi/content/full/ to the aphotic zone. Most recently, it has been hypothesized that the 0904836106/DCSupplemental. 14438–14443 ͉ PNAS ͉ August 25, 2009 ͉ vol. 106 ͉ no. 34 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0904836106 Downloaded by guest on September 30, 2021 A B C D Fig. 2. Modeling parameters of erniettomorphs and rangeomorphs. (A) F Width (a), length (b), and hollowness (c) of an erniettomorph module. (B) GEOLOGY Bipolar addition of erniettomorph module triplets during growth (t ϭ 0, 1, 2…). (C) Overlap (1 ϭ full, 0 ϭ none) between erniettomorph modules was simulated to compare tightly packed vs. loosely overlapping modules. (D) Fractal subdivision of a rangeomorph module. continual spiral, does limit the faithfulness of the model. How- E G ever, the most likely hypothesis was followed, with simulations constructed to add modular units to all three petaloids simul- EVOLUTION Fig. 1. Modular Ediacara fossils. (A) Three incomplete specimens of the erni- taneously (as triplets) and bipolarly (Fig. 2B). Modular units ettomorph fossil Pteridinium composed of tubular modular units. (B) Pteridinium were assumed to have a square cross-section and modeled to with nine modular units (right side of fossil). (C) Erniettomorph Ernietta with evaluate changes in SA/V ratios associated with the size (length module infilling. (D) Magnified section of the specimen in the boxed section in C, and width), number, hollowness, and degree of overlap between with arrows highlighting sediment infill. (E) Rangeomorph fossil Rangea with units (Fig. 2). Unit size and number of units were varied fractal modules (bracket on the right). (F) Rangea with three primary fractal individually and incrementally, as guided by specimen measure- modules (large modules on the left) and three smaller subsidiary modules tucked in between the larger modules. (G) Rangeomorph Fractofusus with 16 fractal ments reported previously (6): width (a: 2.2–4 mm, varied at modules on either side of the longitudinal midline. Bracket displaying one 0.2-mm intervals; Fig. 2A), length (b: 40–85 mm, varied at 5-mm module. G is provided by G.M. Narbonne. (Scale bar: 1 cm.) intervals; Fig. 2A), and number of units (40–85 triplets, varied at five-triplet intervals; Fig. 2B). The thickness of the active biological organic matter was evaluated for a module of average complete specimens suggests that increases in size result from size (length: 55 mm, width: 3.2 mm; n ϭ 11) from the starting