When is a loss a gain? Decoding annelids dietary secrets ~630 million years ago

Explore our Nature Communications study unraveling annelids' ancient secrets. We decode sterol evolution in animals’ ancient ancestor at the dawn of their evolution.
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Sterols, the unsung heroes of life's complexity, can endure within geologic sediments for staggering periods, a striking ~818 million years longer than DNA. Fossil sterols are commonly referred to as “biomarkers”, and are  of interest to many in astrobiology for their use as a proxy for life on other planets. In paleobiology, there is a relatively young field that employs techniques from molecular biology and organic geochemistry to phylogenetically constrain biomarker signals by their relative abundances. One of the earliest signals is the sudden appearance of abundant complex biomarkers containing 28 or more carbons (C28+) around 630 million years ago. Until recently, C28+ biomarkers were considered a signal for fungi or green algae.  In our latest study published in Nature Communications, we wanted to explore the recently described ability of annelid worms to synthesize these complex compounds and the implications for our understanding of the ancient biomarker record.

Challenging Assumptions with Open Minds

Steranes, the fossilized remnants of sterols, have long been the guiding lights of ancient life studies. Traditionally, C27, C28, and C29 steranes were linked to ancient red algae, fungi, and green algae. Like red algae, modern eumetazoans, the group containing annelids, predominantly use cholesterol as well, a C27.  Enter the unexpected protagonist: the 24-C sterol methyltransferase (smt) gene discovered in annelid worms, challenging the conventional narrative of C28+ steranes. Our recent paper delves into the evolutionary history of the smt gene in animals, challenging assumptions about its origin and inheritance.

The Case for Vertical Descent and Room to Grow

Researchers from the Max Planck Institute for Marine Microbiology in Germany recently discovered that gutless marine annelid, Olavius algarvensis, predominantly synthesize sitosterol—a C29 sterol, in a departure from typical animal sterol patterns. Utilizing multiomics, metabolite imaging, and enzyme assays, they identified an SMT responsible for sitosterol synthesis in these animals, challenging conventional views on sterol production in the animal kingdom. This work interpreted the presence of smt’s in annelids as being inherited vertically between eukaryotes. Simultaneously, we independently confirmed the presence of smts in annelid worms, specifically the annelid Capitella Teleta. Our findings point to a different conclusion surrounding the inheritance of smt genes in eumetazoans.

Our vetting of SMTs in public databases like NCBI suggests that many of these genes that supposedly transferred horizontally into animals  are contaminants. Furthermore, our new molecular clock analysis points to a Neoproterozoic radiation of the gene in Eumetazoa, over 541 million years ago. This evidence, when put together, signals an ancient origin for SMTs in the animal lineage. We suggest the scarcity of complex sterol synthesis in most living eumetazoans is the result of extensive gene loss rather than horizontal gene transfer. Our work raises questions surrounding the evolutionary advantages of complex sterol synthesis and loss across diverse lineages. For example, why did at least seven major animal groups relinquish this crucial gene? Our exploration leads us to propose that extensive gene losses across various lineages played a pivotal role, signaling a profound shift in our understanding of the sterols synthesized by the earliest animals. This work motivates a greater impetus for research into the specific functions of smt genes in different species.

Ancestral Traits and Ancient Feeding Strategies

Our research suggests that the ability to synthesize complex sterols is an ancestral trait in animals and prompts a reconsideration when encountering C28+ steranes in eumetazoan fossils. It encourages us to explore the possibility that these organisms might have been synthesizing higher sterols, adding layers of complexity to the interpretation of ancient biomarker records. After surveying the retention and duplication of smt genes in certain animal lineages, we found ourselves grappling with many questions such as why do a small number of animals keep this gene? And in some groups (rotifers, hesionoid worms) they even have multiple copies!

The end of the Neoproterozoic was a pivotal period in the history of life, marked by global warming, ocean oxygenation, and the breakup of the supercontinent Rodinia. These environmental changes likely played a crucial role in shaping the feeding strategies of early animals. As microbial eukaryotes flourished, offering a novel food source for sterols, early animals underwent a significant shift in feeding strategies. Our proposal that many early animal groups independently abandoned sterol modification around the end-Neoproterozoic reflects the influence of environmental shifts and the diversification of eukaryotic prey.

Molecular Echoes of the Neoproterozoic Era

Originating as post-doctoral work in the Summons Lab at MIT and completed at UC Davis in the Gold Lab, our research challenges notions about sterol evolution in early animals. It prompts a reevaluation of the significance of complex sterols in ancient biomarker records and underscores the need for a nuanced understanding of early animal feeding strategies. As we unravel ancient secrets encoded in molecular fossils, these studies open new doors for exploring the evolutionary history of animals, encouraging deeper dives into the mysteries of ancient sterol biosynthesis. All code used for identifying and vetting smts available on our lab GitHub page. And stay tuned for future work exploring bacterial candidates for Neoproterozoic C28+ sterols by Malory Brown.

Two photos of first and second authors, Tessa Brunoir and Christopher Mulligan performing experiments in the Gold Lab at UC Davis
Images of first and second author's Tessa Brunoir and Christopher Mulligan of the paper Common origin of sterol biosynthesis points to a feeding strategy shift in Neoproterozoic animals, performing experiments in the Gold Lab at UC Davis.

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Evolutionary Biology
Life Sciences > Biological Sciences > Evolutionary Biology
Sterols
Life Sciences > Biological Sciences > Chemical Biology > Lipidology > Lipids > Sterols
Sterols
Physical Sciences > Chemistry > Biological Chemistry > Lipidology > Lipids > Sterols
Molecular Genetics
Life Sciences > Biological Sciences > Genetics and Genomics > Molecular Genetics

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