The role of symbiosis in the first colonization of the seafloor by macrobiota: Insights from the oldest Ediacaran biota (Newfoundland, Canada)

Were the First Trace Fossils Really Burrows or Could They Have Been Made by Sediment-Displacive Chemosymbiotic Organisms?

“…One of the most distinctive aspects of the earliest Ediacaran soft-bodied macrobiotas is that-with few rare exceptions-they were immotile, and in many cases grew to very large sizes on matgrounds (Narbonne & Gehling 2003;Liu et al 2016;Taylor et al 2021; Fig. 1b).…”

“…Being immotile on a porous organic-rich seafloor potentially results in serious biogeochemical challenges in the form of hydrogen sulfide buildup below the body tissues (Ortega et al 2008;Dufour & McIlroy 2017a, b). If hydrogen sulfide accumulates unchecked next to the epithelium of an immotile recliner it would likely cause cell-death, meaning that soft-bodied Ediacaran organisms must have been able to modify the organism-substrate interface in a manner that detoxified, or otherwise mitigated, sulfide toxicity (McIlroy et al 2021). Other strategies that animals employ to allow growth on sulfidic porewater substrates involve creation of an inert barrier between the sediment and the organism such as the holdfasts of Crinoids (Seilacher & MacClintock 2005), the basipinacocytes of sponges (Dufour & McIlroy 2017b), or the mucous burrow linings of burrowers that make permanent dwellings (e.g.…”

“…There are many common ectoand endo-symbioses between sulfur oxidizing bacteria and animals, particularly on high surface area, oxygen-rich, epithelia such as gills (Dufour 2005;Dubilier et al 2008). The earliest examples of Ediacaran fossils include the epibenthic Rangeomorpha, some of which had fractal-like lower surfaces and lived reclined on the seafloor (Hawco et al 2020;McIlroy et al 2020McIlroy et al , 2021; Fig. 1d).…”

“…Some rangeomorphs actively displaced sediment during growth such that they grew slightly below the ambient sediment-water interface (Droser et al 2014) and as such were likely adapted to exploit sedimentary biogeochemical gradients, especially the very large reclining organisms (e.g. Bradgatia (see Liu et al 2016) and Gigarimaneta (Taylor et al 2021)). Fractal-like morphologies in reclining organisms are most consistent with sedimentary nutrient exploitation via symbioses with lithoautotrophic bacteria, based around the metabolism of methane, hydrogen, and hydrogen sulfide in particular.…”

“…If the paradigm for a rangeomorph-like symbiotic lifestyle (McIlroy et al 2021) can be extended to unbranched, high surface area-volume ratio burrows without evidence of burrowing action/feeding, then the atypical nature of the earliest trace-fossil biotas and their overlap with the Ediacaran biotas might be explainable.…”