Cryptogamic ground covers as analogues for early terrestrial biospheres: Initiation and evolution of biologically mediated proto-soils.

Affiliation

Mitchell RL(1)(2), Strullu-Derrien C(1)(3), Sykes D(4)(5), Pressel S(6), Duckett JG(6), Kenrick P(1).
Author information:
(1)Earth Sciences Department, The Natural History Museum, London, UK.
(2)Sheffield Tomography Centre
(STC), Kroto Research Institute, The University of Sheffield, Sheffield, UK.
(3)Institut de Systématique, Evolution, Biodiversité
(ISYEB), UMR7205, Muséum National d'Histoire naturelle, Sorbonne Université, CNRS, Paris, France.
(4)Imaging and Analysis Centre
(IAC), The Natural History Museum, London, UK.
(5)Henry Moseley X-ray Imaging Facility, School of Materials, The Royce Institute, The University of Manchester, Manchester, UK.
(6)Life Sciences Department, The Natural History Museum, London, UK.

Abstract

Modern cryptogamic ground covers (CGCs), comprising assemblages of bryophytes (hornworts, liverworts, mosses), fungi, bacteria, lichens and algae, are thought to resemble early divergent terrestrial communities. However, limited in situ plant and other fossils in the rock record, and a lack of CGC-like soils reported in the pre-Silurian sedimentological record, have hindered understanding of the structure, composition and interactions within the earliest CGCs. A key question is how the earliest CGC-like organisms drove weathering on primordial terrestrial surfaces (regolith), leading to the early stages of soil development as proto-soils, and subsequently contributing to large-scale biogeochemical shifts in the Earth System. Here, we employed a novel qualitative, quantitative and multi-dimensional imaging approach through X-ray micro-computed tomography, scanning electron, and optical microscopy to investigate whether different combinations of modern CGC organisms from primordial-like settings in Iceland develop organism-specific soil forming features at the macro- and micro-scales. Additionally, we analysed CGCs growing on hard rocky substrates to investigate the initiation of weathering processes non-destructively in 3D. We show that thalloid CGC organisms (liverworts, hornworts) develop thin organic layers at the surface (<1 cm) with limited subsurface structural development, whereas leafy mosses and communities of mixed organisms form profiles that are thicker (up to ~ 7 cm), structurally more complex, and more organic-rich. We term these thin layers and profiles proto-soils. Component analyses from X-ray micro-computed tomography data show that thickness and structure of these proto-soils are determined by the type of colonising organism(s), suggesting that the evolution of more complex soils through the Palaeozoic may have been driven by a shift in body plan of CGC-like organisms from flattened and appressed to upright and leafy. Our results provide a framework for identifying CGC-like proto-soils in the rock record and a new proxy for understanding organism-soil interactions in ancient terrestrial biospheres and their contribution to the early stages of soil formation.