Hidden decomposers: Revisiting saprotrophy among soil protists and its potential impact on carbon cycling

Abstract

Soil protists are increasingly recognized as key players in organic matter turnover, yet their role as direct decomposers (i.e., saprotrophs) remains underexplored compared to that of bacteria and fungi. Here, we synthesize ecological, physiological, and genomic evidence to highlight the potential of protists to actively decompose organic matter and influence soil carbon cycling. We distinguish two saprotrophic strategies within protists—lysotrophic (extracellular) and phagotrophic (intracellular)—with the latter being unique to protists among microbial decomposers. By directly ingesting particulate or dissolved organic matter, phagotrophic saprotrophic protists may bypass constraints associated with extracellular decomposition, potentially providing an advantage in breaking down recalcitrant substrates. In contrast, lysotrophic saprotrophy in protists involves the secretion of enzymes, similar to bacterial and fungal decomposers. We propose that integrating protist saprotrophy into conceptual and quantitative models of soil organic matter decomposition could address critical knowledge gaps. This integration involves employing functional genomics and functional ecology methodologies to determine, in vitro, the capacity of protists to function as saprotrophs, elucidate the genetic pathways underpinning saprotrophic activities, and assess, in situ, their direct contributions to organic matter decomposition processes. Ultimately, a clearer view of the organic matter decomposition capacities of soil protists will refine our understanding of microbially driven carbon fluxes.