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From Microbial Consortia to Ecosystem Resilience: The Integrative Roles of Holobionts in Stress Biology
Institute for Water Research and Department of Microbiology, University of Granada, CL Ramón y Cajal No. 4, 18071 Granada, Spain
Biology 2025, 14(9), 1203; https://doi.org/10.3390/biology14091203 (registering DOI)
Submission received: 23 June 2025
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Revised: 31 August 2025
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Accepted: 3 September 2025
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Published: 6 September 2025
(This article belongs to the Special Issue Biosynthesis of Metabolites from Microorganisms, or Microorganism-Host Interaction? (Volume II))
Simple Summary
The holobiont framework, encompassing host organisms and their microbial symbionts as integrated biological systems, has revolutionized perspectives on environmental stress responses across diverse taxa. This review synthesizes evidence that holobionts, from plants to animals, rely on microbial partnerships to thrive under environmental challenges. We trace the evolutionary origins of these alliances to ancient microbial consortia, which enabled metabolic innovation and stress resilience. In plants, microbiome-mediated mechanisms (e.g., rhizosphere methanotrophs enhancing drought tolerance) optimize nutrient acquisition and pathogen defense. In animals, the gut microbiota influences systemic health through multi-organ axes (e.g., gut–brain communication via microbial metabolites). Cross-kingdom parallels reveal conserved principles, such as volatile organic compounds (VOCs) facilitating inter-holobiont signaling. Emerging tools, like microbiome engineering, harness these interactions for climate-resilient agriculture and precision medicine. By framing adaptation as a collective trait of the holobiont, this work bridges evolutionary biology, microbiology, and ecology, offering actionable insights for sustainability and health.
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.
