From Microbial Consortia to Ecosystem Resilience: The Integrative Roles of Holobionts in Stress Biology
Maximino Manzanera
Abstract
The holobiont paradigm, conceptualizing host–microbiome assemblages as functionally integrated entities, has fundamentally altered interpretations of adaptive responses to environmental pressures spanning multiple organizational levels. This review synthesizes the current knowledge on microbiome-host coevolution, focusing on three key aspects. First, it examines the evolutionary origins of holobionts from primordial microbial consortia. Second, it considers the mechanistic basis of microbiome-mediated stress resilience in plants and animals. Finally, it explores the ecological implications of inter-holobiont interactions. We highlight how early microbial alliances (protomicrobiomes) laid the groundwork for eukaryotic complexity through metabolic cooperation, with modern holobionts retaining this plasticity to confront abiotic and biotic stressors. In plants, compartment-specific microbiomes (e.g., rhizosphere, phyllosphere) enhance drought tolerance or nutrient acquisition, while in animals, the gut microbiome modulates neuroendocrine and immune functions via multi-organ axes (gut–brain, gut–liver, etc.). Critically, we emphasize the role of microbial metabolites (e.g., short-chain fatty acids, VOCs) as universal signaling molecules that coordinate holobiont responses to environmental change. Emerging strategies, like microbiome engineering and probiotics, are discussed as tools to augment stress resilience in agriculture and medicine. By framing adaptation as a collective trait of the holobiont, this work bridges evolutionary biology, microbiology, and ecology to offer a unified perspective on stress biology.