Ancestral germen/soma distinction in microbes: Expanding the disposable soma theory of aging to all unicellular lineages

Abstract

Life has persisted for about 3.5 billion years (Gy) despite fluctuating environmental pressures and the aging and mortality of individuals. The disposable soma theory (DST) notoriously contributes to explain this persistence for lineages with a clear soma/germen distinction. Beyond such lineages however, the phylogenetic scope of application of the DST is less obvious. Typically, the DST is not expected to explain the survival of microbial species that comprise single-celled organisms apparently lacking a germen/soma distinction. Here, we present an evolutionary argument that generalizes the explanatory scope of DST to the entire microbial world and provides a novel characterization of the deep molecular and evolutionary roots supporting this expanded disposable soma theory of aging. Specifically, we argue that the germen/soma distinction arose early in evolution and identify DNA semi-conservative replication as a critical process through which two forms of rejuvenation could have evolved in the first microbes. Our hypothesis has fundamental and practical implications. First, whereas unicellular organisms were long thought of as potentially immortal, we suggest instead that all unicellular individuals (prokaryotes or protists alike) are very likely to age, either replicatively or physiologically, or both. Second, our theory introduces a profound reconsideration of microbial individuality, whereby, all microbial individuals, as seen by natural selection, present an obligate transient germen/soma distinction during their life cycles. Third, our work promotes the study of cellular division in prokaryotes and in protist mitosis to illuminate the evolutionary origin of the soma and germen division, traditionally studied in animals. These ideas set the stage for progress in the evolutionary theory of aging from a heretofore overlooked microbial perspective.