Possible evolution of mobile animals in association with microbial mats

Abstract

Complex animals first evolved during the Ediacaran period, between 635 and 542 million years ago, when the oceans were just becoming fully oxygenated. In situ fossils of the mobile forms of these animals are associated with microbial sedimentary structures [1][2][3] , and the animal's trace fossils generally were formed parallel to the surface of the seabed, at or below the sediment-water interface 4,5 . This evidence suggests the earliest mobile animals inhabited settings with high microbial populations, and may have mined microbially bound sediments for food resources [6][7][8] . Here we report the association of mobile animals-insect larvae, oligochaetes and burrowing shore crabs-with microbial mats in a modern hypersaline lagoon in Venezuela. The lagoon is characterized by low concentrations of dissolved O 2 and pervasive biomats dominated by oxygen-producing cyanobacteria, both analogous to conditions during the Ediacaran. We find that, during the day, O 2 levels in the biomats are four times higher than in the overlying water column. We therefore conclude that the animals harvest both food and O 2 from the biomats. In doing so, the animals produce horizontal burrows similar to those found in Ediacaran-aged rocks. We suggest that early mobile animals may have evolved in similar environments during the Ediacaran, effectively exploiting oases rich in O 2 that formed within low oxygen settings.Although it is hypothesized that the appearance of the earliest mobile animals (putatively bilaterians) was made possible by the increasing abundance of dissolved oxygen in oceanic waters, dissolved oxygen ∼600 Myr was probably spatially variable and low overall, ranging between 10 and 18% of today's levels 9,10 . To most modern animals, persistently low oxygen concentrations are lethal-suggesting either that the first bilaterians were metabolically different from their modern counterparts, or that they exploited heretofore unrecognized sources of oxygen in the Ediacaran seas. Is it possible that oases of high oxygen concentration were present well before the Ediacaran and that they persisted in Ediacaran shallow marine environments, where photosynthetic biomats produced copious amounts of oxygen that diffused into the adjacent sediment and water column? Modern biomats-discussed belowcommonly have daytime oxygen concentrations that exceed atmospheric levels by several orders of magnitude 11 . This leads us to hypothesize that the first bilaterian animals did not need to evolve the ability to withstand low oxygen concentrations so much as to cope with spatiotemporal variability in oxygen availability.The trace-fossil record of bilaterian metazoans extends to the late Ediacaran about 555 Myr ago 12 (perhaps as early as 565 Myr; ref. 13)

Trace elements at the intersection of marine biological and geochemical evolution

“…This is reflected by a switch from the absence to presence of carbonate-bound iodine (Hardisty et al, 2014). Such a record indicates the potential for habitable marine environments, at least in terms of minimum O 2 thresholds, hundreds of millions of years before the first evidence for animal life or eukaryotic diversification (Gingras et al, 2011;Knoll, 2014).…”

Iron formations: A global record of Neoarchaean to Palaeoproterozoic environmental history

“…Under such a scenario, oxygen produced by the benthic microbial community would be consumed proximal to the mat, much as is observed in some modern mat systems (e.g., Gingras et al, 2011;Sumner et al, 2015).…”

Paleobiological Perspectives on Early Eukaryotic Evolution

“…Moreover, they note that the aggressively oxidizing environments generated diurnally by cyanobacterial oxygen production within mats (e.g., Gingras et al 2011) would have destroyed lipids sourced from the overlying water column. In consequence, the lack of steranes in most Proterozoic shales may simply reflect preservational circumstances common before the Ediacaran Period, when evolving animals dramatically restricted the distribution of benthic mat communities.…”