Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae

Abstract

The acquisition of photosynthesis is a fundamental step in the evolution of eukaryotes. However, few phototrophic organisms are unambiguously recognized in the Precambrian record. The in situ detection of metabolic byproducts in individual microfossils is the key for the direct identification of their metabolisms. Here, we report a new integrative methodology using synchrotron-based X-ray fluorescence and absorption. We evidence bound nickel-geoporphyrins moieties in low-grade metamorphic rocks, preserved in situ within cells of a ~1 Gyr-old multicellular eukaryote, Arctacellularia tetragonala. We identify these moieties as chlorophyll derivatives, indicating that A. tetragonala was a phototrophic eukaryote, one of the first unambiguous algae. This new approach, applicable to overmature rocks, creates a strong new proxy to understand the evolution of phototrophy and diversification of early ecosystems.

Eukaryogenesis and oxygen in Earth history

“…Among a plethora of other candidate archaeplastids around the Mesoproterozoic-Neoproterozoic boundary ca. 1 Ga [94][95][96][97] , there are also claims of Amorphea/Unikonta, such as the putative holozoan Bicellum 98 -though its purported holozoan affinity is not sufficiently robust to use as a fossil calibration point for eukaryote evolution. Claims of fungi at ca.…”

In Living Color: Pigment-Based Microbial Ecology At the Mineral–Air Interface

“…By measuring the nitrogen isotope ratios of porphyrins retrieved in sedimentary rocks, the researchers were able to quantify the abundance of different phototrophs in the ocean, establishing the dominance of cyanobacteria over planktonic algae. Sforna and colleagues ( 2022 ) discovered in situ the first evidence of Chls remnants in a billion-year-old multicellular algal microfossil preserved in shales from the Congo Basin. The result provides new clues about the evolution of eukaryotic phototrophy during the Precambrian and the diversification of primary producers in early ecosystems.…”

Paleobotany to understand evolution and biodiversity in Mexico

“…In this sense, the Sonoran stromatolites call for further comparative studies of the type of sediments and macroscopic and microscopic morphologies that characterize them, to then formulate hypotheses about the type of environments that existed on the shores of that craton in the Proterozoic. Future studies should also search for the presence of microfossils, to explore their quality of preservation and their diversity (e.g., McMenamin et al 1983), considering that photosynthetic eukaryotes were already present in the environment (Sforna et al 2022).…”

“…The description of such microfossil assemblages resulted in the identification of algae, cyanobacteria and benthic and planktonic habits of the different morphospecies, which has enriched the value of this fossil locality. In addition, given their excellent preservation, it is likely that part of their organic matter was preserved, allowing for inferring particular metabolisms (see applications in Sforna et al 2022) and, therefore, details of their biology that otherwise would remain speculative or unknown. Also, numerous plants from these 'Huepac Chert' rocks, such as palm trees and Haloragaceae plants (Cevallos-Ferriz & Ricalde-Moreno 1995, Hernández-Castillo & Cevallos-Ferriz 1999, with the same ultrastructural detail of preservation as the microfossils, have been described.…”

“…Understanding peculiarities of the biology of past plants clarifies that their functioning and associations have changed through time to generate their current biodiversity. Some key aspects of this history include the evolution of photosynthetic organisms (e.g., Sforna et al 2022) and their ability to establish themselves on continents through anchoring and absorption systems (e.g., Lu et al 2020), depending even less on water (Schoen et al 2019), as well as developing conduction systems to move water from the ground to aerial parts.…”