Ediacaran Pre-Placozoan Diploblasts in the Avalonian Biota: the Role of Chemosynthesis in the Evolution of Early Animal Life

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Ediacaran pre-placozoan diploblasts in the Avalonian biota: the role of chemosynthesis in the evolution of early animal life

SUZANNE C. DUFOUR1 & DUNCAN MCILROY2* 1Department of Biology, Memorial University of Newfoundland, St John’s, NL, Canada A1B 3X9 2Department of Earth Sciences, Memorial University of Newfoundland, St John’s, NL, Canada A1B 3X5 *Correspondence: [email protected]

Abstract: The large, enigmatic members of the Ediacaran biota have received much attention regarding their possible afﬁnities and mode of life. Fossil evidence reveals that many Ediacaran animals, such as the rangeomorphs, were characterized by extensive surface areas, lived in close association with the seaﬂoor and were non-motile. We argue for the presence of a simple, diploblastic body plan in these early animals and discuss the means by which they probably derived nutrients from chemosynthetic bacteria thriving at the sediment–water interface. We consider that the large surface area of some Ediacaran organisms in the Avalonian biota may have been an adaptation for maximizing a phagocytotic or chemosymbiotic surface. Ediacaran animals probably increased the availability of oxygen along their ventral surface either by diffusion or ciliary pumping. This increased supply of oxygen to the sediment is inferred to have simultaneously increased the productivity of their food source (chemosynthetic bacteria) and restricted the build-up of toxic sulphides in the pore waters below their bodies. This is an example of a very simple form of ecosystem engineering.

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Some of the earliest known Ediacaran macrofossils The biological affinity of Ediacaran organisms have been found in c. 580 myr-old, deep, sub-photic remains enigmatic, but recent work tends to charac- zone marine deposits in southeastern Newfoundland terize them as stem- or crown-group metazoans and form the so-called Avalonian biota (Narbonne (see Liu et al. 2014, 2015), potentially representing 2005); other early macrofossils, such as those from multiple clades that have been preserved under a the Lantian biota, are of uncertain age (Budd & common taphonomic regime (Xiao & Laflamme Jensen 2015). The majority of the Avalonian macro- 2009). Molecular clock data suggest that the origin biota is represented by non-mineralized epibenthic of metazoans predates the late Ediacaran period, macro-organisms, which, even in the oldest fossi- with many major clades radiating during the Cryo- liferous strata, grew to up to 1 m in length or genian and early Ediacaran (dos Reis et al. 2015; 20 cm in diameter (Narbonne & Gehling 2003; Erwin 2015). There is no convincing direct evidence Liu et al. 2011, 2016; Fig. 1a, b). One of the charac- for triploblastic features and complex internal teristics of this fossil assemblage is that the organ- organs among the Ediacaran macrofossils and a isms were almost exclusively sessile, with only simple diploblastic bauplan consisting of multiple rare surficial metazoan trails in strata c. 565 myr modules along a polarized body axis is typically old and younger (Liu et al. 2010) until the first invoked for these organisms (Laflamme et al. phase of ichnological radiation in the latest Edia- 2009; Budd & Jensen 2015), with the possible caran at c. 550 Ma (Jensen 2003). It would there- exception of the latest Ediacaran mollusc-like Kim- fore seem that for almost 30 myr prior to 550 Ma, berella (e.g. Ivantsov 2009; Vinther 2015). We pro- the seafloor of Avalonia was dominated by large pose that some elements of the soft-bodied Ediacara Ediacaran macro-organisms that were sessile and biota possessed a simple architecture consisting of either (1) epibenthic, reclining on the sediment sur- an epithelial surface enclosing mesenchyme (i.e. face (e.g. Fractofusus; Fig. 1c) or tethered to it by inert, predominantly acellular material), similar to a discoidal surficial holdfast (e.g. Charniodiscus the body plan of extant placozoans, as has been Laflamme et al. 2004; Fig. 1d) or (2) hemibenthic, proposed for the motile late Ediacaran organism having a bulbous holdfast within the sediment Dickinsonia (Sperling & Vinther 2010). An impor- (e.g. Trepassia Brasier et al. 2013; Fig. 1a, e). tant difference between the placozoan model for

From:Brasier A. T., McIlroy D. & McLoughlin, N. (eds) Earth System Evolution and Early Life: a Celebration of the Work of Martin Brasier. Geological Society, London, Special Publications, 448, http://doi.org/10.1144/SP448.5 # 2016 The Author(s). Published by The Geological Society of London. Publishing disclaimer: www.geolsoc.org.uk/pub_ethics Downloaded from http://sp.lyellcollection.org/ by guest on September 30, 2021

S. C. DUFOUR & D. MCILROY

Fig. 1. The earliest Ediacaran macrofossils from (a, b) the Drook Formation, (c, d) the Mistaken Point Formation and (e) the Trepassey Formation of southeastern Newfoundland. (a) Trepassia wardae, a large frondose Ediacaran organism (scale bar 5 cm). (b) Large ivesheadiomorph fossils up to 20 cm in diameter considered to represent decayed remnants of the Ediacaran biota (scale bar 4 cm). (c) Fractofusus misrai showing fractal-like rangeomorph-type branching (scale bar 4 cm). (d) Charniodiscus showing the basal holdfast, stem and frond that could have been periodically held into the water column for oxygen collection (scale bar 4 cm). (e) Holdfast of a frondose Ediacaran showing that the holdfasts of some taxa were anchored within the sediment (scale bar 4 cm).

Dickinsonia and the characteristics of the earliest move away to ﬁnd additional food, but also to Ediacaran biotas, as described in this paper, is the avoid the build-up of sulphide in the pore waters immobility of the latter, which constrains their pos- beneath it (Loenarz et al. 2011; cf. McIlroy et al. sible modes of feeding. 2009). Feeding using a placozoan-like ventral diges- Extant placozoans lack a digestive system and tive sole has been proposed as a stage in meta- therefore cannot support ingestive feeding modes. zoan evolution that predates the evolution of a gut Instead, cells from the lower epithelium secrete (Arendt et al. 2015). Motile placozoans such as exoenzymes that lyse surﬁcial microalgae in mat- Trichoplax use ciliary gliding and amoeboid move- grounds and the resultant breakdown products of ment following the local digestion of microbial extracellular digestion are absorbed by ventral mats, as is invoked for the Ediacaran organisms cells (i.e. the ‘digestive sole’) for nutrition (Smith Yorgia and Dickinsonia (Ivantsov & Malakovskaya et al. 2014, 2015a). Once the matground food 2002; Dzik 2003; Fedonkin 2003; Gehling et al. resource has been exploited, the placozoan must 2005; Seilacher 2007; Sperling & Vinther 2010) Downloaded from http://sp.lyellcollection.org/ by guest on September 30, 2021

PRE-PLACOZOAN EDIACARANS on the basis of Epibaion trace fossils (Ivantsov sedimentary biomass from matgrounds and pelagic 2013). However, immobile Ediacaran forms must fallout (McIlroy & Logan 1999). Sulphidic pore have used a different feeding strategy that required waters at the seafloor pose significant metabolic no motility. challenges to immotile epifaunal and hemibenthic organisms such as the early Ediacaran biota due to the toxicity of pore water sulphides. Common Feeding strategies of Ediacaran organisms microbial inhabitants of redoxclines include chemo- Most previous interpretations of the feeding strate- lithoautotrophs, such as the sulphur-oxidizing bac- gies of sessile Ediacarans focused on either suspen- teria that derive energy for carbon fixation from the sion feeding/filter feeding (the uptake of particulate oxidation of reduced sulphur (e.g. Howarth 1984). organic matter) or osmotrophy, i.e. the uptake of The likely abundance of sulphate-reducing bac- dissolved organic matter (DOM). These interpreta- teria close to the seafloor means that the immotile tions are founded in the large-scale morphological Ediacaran organisms must have developed adapta- similarities between frondose Ediacarans and sea tions to reduce the impact of sulphide on the ventral pens. The former have been broadly considered to epithelium. Considering that oxygen was available, be suspension feeders (e.g. Clapham et al. 2003), at least periodically, in the overlying water (Hood & but this has been shown to be inaccurate (Antcliffe Wallace 2014; Wood et al. 2015; Cui et al. 2016; & Brasier 2007); more recent computational models Sahoo et al. 2016), the upper surface of Ediacaran support passive suspension feeding in the enig- organisms is likely to have been adapted for oxy- matic Tribrachidium (Rahman et al. 2015). How- gen uptake. Oxygen transport could have occurred ever, clear evidence for the presence of pores within a diploblastic Ediacaran animal by diffusion allowing the uptake of particulate matter is cur- through the mesenchyme, which could also have rently lacking (Liu et al. 2015). Alternatively, DOM stored oxygen during periods of hypoxia, as demon- could be absorbed through cell surfaces, as has been strated in the mesoglea of modern scyphomedusae proposed for Ediacaran forms with large surface (Thuesen et al. 2005; Pitt et al. 2013). Alternatively, areas such as rangeomorphs (Laflamme et al. 2009). in frondose or plicate taxa, ciliary pumping could Although DOM uptake may be theoretically feasi- lead to the transport of oxygenated water to the ble in Ediacaran organisms if the metabolically ventral surface (Fig. 2). The net effect of diffusion active layers are fairly thin (Laflamme et al. 2009), and/or the ciliary transport of oxygen to the ventral it remains questionable whether the size and quality surface of Ediacaran organisms would be to enhance of the DOM reservoir were sufficient to sustain such the productivity of chemolithoautotrophs in the pore large organisms using osmotrophy alone (Johnston water system near the organism (McIlroy & Logan et al. 2012; Liu et al. 2015). 1999). It would also oxidize the sulphides in pore It has been proposed that Ediacaran organisms waters and thereby avoid tissue damage. We con- could also have relied on symbionts as a source of sider it likely that this closely integrated microbe– nutrients, a hypothesis that has largely been rejected macrobiotic biogeochemical interaction created a because photosymbiosis could not be supported food resource for the Ediacaran macrobiota and in the deep-water marine setting of the Avalonian may have fuelled their large size. The derivation Ediacaran biota given the low availability of light. of nutrition from the sedimentary microbiota by Chemosymbiosis has also occasionally been con- immotile Ediacaran organisms, such as the rangeo- sidered as a possible feeding mode for Ediacaran morphs, could have been achieved in a number of organisms (Seilacher 1984; McMenamin & McMe- different ways using some combination of phagotro- namin 1990; McMenamin 1998; Liu et al. 2015), phy and chemosymbiosis. but has been dismissed partly on the grounds that the inferred tiering of the Avalonian biota is similar Phagotrophy to modern suspension feeding communities and does not show the patchiness expected of (pre- Immotile Ediacaran macro-organisms such as sumably vent-related) chemosynthetic communities the sediment-reclining form Fractofusus (Fig. 1c) (Laflamme & Narbonne 2008). could have efficiently acquired nutrients from che- molithoautotrophic microbes through non-ingestive processes, including the use of the high surface area Chemosynthetic feeding modes in ventral epithelium as a phagocytotic surface (Fig. 2). Ediacaran organisms Phagotrophy, the uptake and subsequent digestion of larger particles such as microbes and particulate In the absence of significant surficial bioturbation matter, is a fundamental property of eukaryotes prior to about 550 Ma (Jensen 2003), a redoxcline (Fenchel 2012). Supporting evidence for such a would have developed at the sediment–water inter- mode of life in certain rangeomorphs is provided face due to microbial sulphate reduction of the by the field observation that Fractofusus commonly Downloaded from

hydrogen sulphide + methane hydrogen sulphide + methane hydrogen sulphide + methane hydrogen sulphide + methane http://sp.lyellcollection.org/ .C UOR&D MCILROY D. & DUFOUR C. S. byguestonSeptember30,2021

Fig. 2. Diagrammatic reconstruction of the quilted fractal-like branching of the immotile Ediacaran taxon Fractofusus showing details of the means by which the organism might have interacted with the underlying substrate. The lower diagram shows the oxygenation of the lower surface using waves of ciliary contraction and diffusion. The supply of oxygen is likely to have stimulated microbial productivity in the adjacent sediment. The top row shows different possible modes of feeding for the immotile Ediacaran organisms. Green circles represent the distribution and abundance of chemolithoautotrophs and the curved arrows show the diffusion of solutes. From left to right the modes of feeding depicted are: phagotrophy, with irrigation using cilia; ectosymbiosis; endosymbiosis; and endosymbiosis in a trophosome, which would require a thin organism and the diffusion of sulphide/methane throughout the organism. POM, particulate organic matter. Downloaded from http://sp.lyellcollection.org/ by guest on September 30, 2021

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Trichoplax secretes mucus to: (1) facilitate ciliary locomotion; (2) provide a substrate for micro-algal digestion; and (3) allow the cilia of the ventral surface to produce both co-ordinated motility and the churning action that facilitates ingestion (Smith et al. 2015a). The epithelium of chemosynthetic phagotrophs, in contrast, requires a less complex grade of organization because no glandular cell is required for exoenzyme production. Epithelial surfaces of immotile Ediacaran chemosynthetic phagotrophs could, at their simplest, consist of cells with an apical microvillar layer, specialized in nutrient uptake. Chemosynthetic phagotrophy could therefore be considered to be an evolutionary precursor to the placozoan grade of organization, characterized by a digestive ventral epithelium (Arendt et al. 2015) that requires, in its most simple form, mucociliary motility to ﬁnd new food resources.

Fig. 3. Large Fractofusus overlying a circular Chemosymbiosis ivesheadiomorph considered to be a necromass that created hotspots of chemosynthesis on the seafloor A wide variety of extant macroinvertebrates analogous to modern whale falls. Note that other living at the interface between oxic and anoxic small Fractofusus are also associated with the iveseheadiomorph (scale bar 5 cm). environments gain nutrients from chemoautotrophic sulphur-oxidizing and/or methanotrophic bacteria (Duperron et al. 2005; Dubilier et al. 2008). Although some animals graze on these microbes, grow on ivesheadiomorphs (Fig. 3), which are con- an ingestive process that is comparatively metabol- sidered to represent local concentrations of necro- ically expensive, others have evolved symbioses mass (Liu et al. 2011). Such hotspots of microbial with chemolithoautotrophs in which the host typi- productivity were created by the decomposition of cally provides oxygen to, and directly obtains nutri- earlier generations of Ediacarans that lived on the ents from, populations of bacteria (Dubilier et al. same surface (Liu et al. 2011). Ivesheadiomorphs 2008). Extant macro-organisms with chemosymbi- might therefore be considered as the Ediacaran ana- otic feeding strategies (e.g. thiotrophy and methano- logue of modern whale falls that are loci of chemo- trophy) are anatomically more complex and include synthesis on the modern seafloor (Krogh 1934; organs and tissue types that cannot be confidently Budd & Jensen 2015; Smith et al. 2015b). We note inferred from the majority of even the best-pre- that few other taxa in the Mistaken Point biota grew served Ediacaran organisms (Brasier & Antcliffe on top of other Ediacaran organisms and that Frac- 2008). It is possible, however, that organisms with tofusus was not readily transported (Gehling & much simpler, gutless body plans could also be Narbonne 2007), so the association is unlikely to chemosymbiotic. be accidental. Most known chemosymbiotic animals maintain Animals that feed by phagotrophy, such as the their symbionts within cells (Dubilier et al. 2008). Porifera, may attain large sizes even in the absence Others, such as thyasirid and some bathymodiolid of a digestive tract provided that they have a large bivalves, establish extracellular symbioses with internal surface area (e.g. canals lined with choano- thiotrophic and/or methanotrophic chemolithoauto- cytes) for feeding. In contrast with the Porifera, trophic bacteria that they phagocytose for intracellu- many sessile Ediacaran forms such as Fractofusus lar digestion (Dufour 2005; Duperron et al. 2005). and Charniodiscus (Fig. 1c, d) have a large external Extracellular symbioses are generally considered to surface area that could also be involved in microbial be simpler than endocellular symbioses (Smith 1979; phagocytosis. Epithelial surfaces involved in che- Rosati 2004), but both types could have existed mosynthetic phagotrophy require fewer cell types among the immotile elements of the Ediacaran biota than a placozoan-like mucociliary sole that releases (Fig. 2). Endocellular symbionts could be main- exoenzymes. Animals at the gastraeal or pre-gas- tained in either (1) the ventral epithelial cells of Edi- traeal grade of organization have four cell types: acaran organisms such as Fractofusus that lie on the mucocytes, glandular cells for digestive enzyme seafloor (Fig. 2) or (2) in an internal mass of cells production, ciliary cells, and cells specialized in analogous to the trophosome of the mouthless flat- nutrient uptake (Arendt et al. 2015). The placozoan worm Paracatenula, which has been described as Downloaded from http://sp.lyellcollection.org/ by guest on September 30, 2021

S. C. DUFOUR & D. MCILROY the most primitive chemosymbiotic animal known facilitates the growth of large organisms with a (Gruber-Vodicka et al. 2011; Fig. 2). Ectosymbionts high surface area to volume ratio, such as character- associated with Ediacaran organisms could either izes the Ediacara biota. Very large surface areas have been associated with the ventral surface of enable high rates of metabolite and waste product reclining forms that were constantly in contact diffusion and are the most important characteristic with the seafloor (Fig. 2), or possibly with the sur- of the symbiont-bearing organs of extant chemo- face of fronds that were episodically held in contact symbiotic animals (e.g. bivalve gills; Childress & with the seafloor (see Fig. 4). Girguis 2011). Chemosymbiosis or chemoautotroph The fractal-like growth patterns of permanently phagotrophy could thereby explain the hitherto sessile reclining Ediacaran organisms such as Frac- unresolved conundrum of why the first fossil organ- tofusus (Seilacher 1992; Gehling & Narbonne 2007) isms were so large (Narbonne 2011). that maximize the ventral surface area of the The giant epibenthic ectosymbiotic colonial cil- organism are considered here to be adaptations for iate Zoothamnium niveum (Bauer-Nebelsick et al. chemosynthetic feeding or symbiosis (Fig. 1c, 2). 1996; Rinke et al. 2006) had a uniaxial frond-like Otherwise, the growth of extensive surfaces in direct morphology (Kloiber et al. 2009; Fig. 4) that is contact with reducing pore waters makes no logical superficially reminiscent of the frondose Ediacaran sense. Chemosynthetic feeding modes require no taxa (e.g. Laflamme et al. 2004; Fig. 1d), as noted gut and are energetically efficient because there is previously (McMenamin 1998). The epithelial sur- no production of exoenzymes as required by the faces of Zoothamnium niveum, like those of chemo- mucociliary digestive sole of a placozoan grade synthetic phagotrophs, contain few specialized cell organism (Sperling & Vinther 2010; Arendt et al. types and are densely covered in ectosymbionts 2015). A phagotrophic or chemosymbiotic organ- (Bright et al. 2014). Zoothamnium actively modu- ism does not need to compete with smaller eukary- lates the redox conditions experienced by its thio- otes or prokaryotes for the products of extracellular trophic ectosymbionts by alternately raising its digestion. Intracellular symbiosis, in particular, is frond into the water column to harvest oxygen, highly ecologically efficient and can support the before returning the frond to a reclining position growth and metabolism of large gutless organisms on the sulphide-rich seafloor (Bauer-Nebelsick living at the redoxcline; however, the maintenance et al. 1996; Bright et al. 2014). Tentative evidence of high growth rates in large chemosymbiotic ani- for multiple impressions of a frondose Ediacaran mals such as the vent tubeworm Riftia pachyptila organism are known from Newfoundland (McIlroy requires adaptations for supplying oxygen to symbi- et al. 2009; Fig. 4a, c) and may support the role of onts (Childress & Girguis 2011). Mesoglea-rich dip- early Ediacaran fronds as an oxygen-collecting loblastic organisms have both a low oxygen demand and symbiont-hosting organ used in the same man- and a low carbon content (Pitt et al. 2013), which ner as the frond of Zoothamnium (Fig. 4b, c).

Fig. 4. Evidence for the use of fronds in chemosymbiosis. (a) Multiple impressions of closely associated fronds from the trace fossil bed at Mistaken Point, Newfoundland (Liu et al. 2010). Note the multiple impressions of the margin of fronds 1 and 2 and that frond 3 is anchored within the sediment, i.e. without a surﬁcial disc. (b) Diagrammatic representation of the modern ciliate Zoothamnium, the frondose portion of which is covered in abundant thiotrophic bacteria in an ectosymbiotic relationship. (c, d) Model to demonstrate how the mode of life of Zoothamnium might apply to Ediacaran frondose rangeomorph taxa and the multiple impressions in part (a). Downloaded from http://sp.lyellcollection.org/ by guest on September 30, 2021

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Conclusions additional work, be extended to many younger Ediacaran taxa. The younger Ediacaran sections Our assessment of the mode of life of the earliest were mostly deposited in comparatively shallow rangeomorph elements of the Ediacaran biota in water and appear to contain an intermediate biota Avalonia suggests the following. between the Ediacaran Avalon biota and the typical (1) They were immotile diploblastic animals with biomineralized Cambrian biotas. They include a a pre-placozoan grade of organization and mixture of motile and immotile organisms in eco- lived below the photic zone. This is consistent systems that need careful reassessment in the light with other recent arguments that suggest that of our findings. the stratigraphically much younger, shallow Dickinsonia This work was partly inspired by the late Professor Martin marine Ediacaran was of placo- Brasier, who sadly did not live to see it to fruition. We ded- zoan grade, had a mucociliary sole and fed icate this paper to his memory. This work was supported by on photosynthetic microbial mats using extra- NSERC Discovery Grants to both authors and benefited cellular digestion (Sperling & Vinther 2010). from the thoughtful review of Soren Jensen and an anony- (2) The high surface area of the ventral surface of mous reviewer. many elements of the oldest Ediacaran biota in southeastern Newfoundland, especially rangeomorphs such as Fractofusus, is most con- References sistent with either microbial phagotrophy or the presence of extracellular or intracellular Antcliffe, J.B. & Brasier, M.D. 2007. Charnia and sea chemosymbionts. Such feeding modes are pens are poles apart. 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