The Plant‐Microbe Alliance for Environmental Restoration: From Nature‐Inspired Solutions to Engineered Ecological Recovery

ABSTRACT

According to the United Nations, up to 40% of the world‘s terrestrial ecosystems are degraded and in need of ecological restoration. Here, we argue that ecosystem restoration requires not only the reintroduction of plant species but also the recovery of the biological interactions that sustain ecosystem functioning. Plants and their associated microbiomes form integrated functional units in which microorganisms contribute to nutrient cycling, stress tolerance, contaminant degradation and ecosystem resilience. These plant–microbe partnerships therefore represent a new opportunity for environmental biotechnology. Advances in microbiome engineering, multi‐omics and artificial intelligence are enabling the identification, design and management of microbial communities with complementary functions adapted to specific restoration contexts. However, the complexity of environmental microbiomes, the technical limitations of multi‐omics in contaminated environments and the gap between computational predictions and ecological performance highlight the need for experimental and field‐scale validation. In this context, we propose Holobiont Engineering for Ecosystem Restoration (HEER) as a conceptual framework that treats plants and their microbiomes as functional units and makes ecological interactions explicit targets of restoration. This perspective positions microbial biotechnology at the interface between ecological restoration and environmental engineering, supporting a shift from species‐focused approaches towards the recovery of ecosystem functions.

Conceptual transition from traditional plant‐centred restoration approaches towards holobiont engineering for ecosystem recovery. While early restoration strategies primarily focused on plant establishment, accumulating evidence demonstrates that ecosystem resilience depends on functional interactions between plants and their associated microbiomes. Emerging technologies, including multi‐omics, synthetic ecology, and artificial intelligence, may enable the design of plant‐microbiome systems capable of enhancing pollutant removal, carbon sequestration, biodiversity recovery, and climate resilience.

1. The Need for Environmental Restoration

Anthropogenic activities have perturbed environments, severely limiting their capacity for natural regeneration. Land degradation, pollution, biodiversity loss and climate change are now recognized as interconnected challenges affecting ecosystem functioning. Therefore, there is an urgent need not only to restore the degraded landscape but also to design new types of urban and natural spaces that can support ecosystem functioning and resilience (Klaus and Kiehl 2021).

According to the United Nations, up to 40% of the world's terrestrial ecosystems are degraded, affecting the well‐being of billions of people and compromising food production, water security and climate resilience (UNEP 2023). Soil pollution is a widespread global problem resulting from industrial activities, mining, unsustainable agricultural practices, waste disposal, and other anthropogenic pressures (FAO and UNEP 2021). Since the beginning of the 21st century, global annual production of industrial chemicals has doubled to approximately 2.3 billion tons and is projected to increase by 85% by 2030. During the same period, pesticide use increased by 75% between 2000 and 2017, while global waste generation currently reaches approximately 2 billion tons annually and is projected to increase to 3.4 billion tons by 2050 (FAO and UNEP 2021). These pressures contribute to the accumulation and persistence of diverse contaminants in soils, including heavy metals, pesticides, hydrocarbons, plastics, pharmaceuticals, antimicrobials and other emerging pollutants. Beyond their direct toxic effects, such contaminants can alter soil properties and biological communities, impair ecosystem functioning, reduce biodiversity, affect water and food systems and generate risks to human health (FAO and UNEP 2021; Zhu et al. 2026). The launch of the UN decade on Ecosystem Restoration (2021–2030) further highlights the urgency of accelerating ecosystem recovery at a global scale (UNEP, 2021).

The complexity of the causes and solutions of environmental challenges has reinforced the need for a holistic view of environmental recovery. In this context, the concept of “biocomplexity,” defined as “the interdependence of elements within specific environmental systems, and the interactions between different types of systems” (Artiola et al. 2004), is fully recognized, emphasizing that ecosystem restoration cannot be achieved by addressing physical, chemical and biological processes independently. Instead, successful restoration requires the understanding of recovering the interactions that sustain ecosystem functioning.

Environmental remediation and restoration are closely related. Although remediation focuses on contaminant removal while restoration aims to recover ecosystems, the two concepts are practically inseparable in real‐world projects. Historically, restoration efforts have focused on rebuilding plant communities. Contaminated soils have been revegetated, degraded landscapes have been stabilized and vegetation cover has been used as a key indicator of restoration success. However, this simplified approach has often resulted in suboptimal outcomes due to inadequate stakeholder engagement, poor site assessment, insufficient invasive‐species control, inappropriate species selection, a lack of long‐term monitoring, and, importantly, the neglect of microbial communities associated with plants (Koziol et al. 2018; Höhl et al. 2020; Larson et al. 2022; Zhu et al. 2026).

Furthermore, environmental degradation rarely results from a single stressor. Chemical pollution, chronic exposure to antibiotics and pesticides, widespread selection for antimicrobial resistance, land‐use change, and intensifying climate change can act simultaneously and modify microbial communities through changes in habitat conditions, trophic and host–microorganism interactions, and altering dispersal and recovery dynamics (Wood et al. 2026).

2. The Plant‐Microbe Partnership Paradigm

Plants and their associated microbiota are integrated biological units, commonly referred to as holobionts (Trivedi et al. 2020; Vandenkoornhuyse et al. 2015). Consequently, plant physiology is shaped by complex interactions with bacteria, fungi, archaea and other microorganisms inhabiting the rhizosphere, endosphere and phyllosphere (Berendsen et al. 2012; Compant et al. 2019). These microbial communities influence nutrient acquisition, stress tolerance, pathogen suppression, carbon cycling and numerous other processes essential for ecosystem functioning.

The recognition of plants as holobionts has had profound implications for restoration ecology: plant‐associated microbial communities should be considered active drivers of restoration outcomes rather than passive components of recovering environments (Guerra et al. 2020; Robinson et al. 2023; Yuan et al. 2025). As evidence accumulates across diverse ecosystems, a new paradigm is emerging. Successful restoration may depend not only on reintroducing plants but also on restoring the microbial partnerships that enable them to establish, adapt and thrive under environmental stress (Robinson et al. 2023).

3. Plant‐Microbe Partnerships for Restoration

Beyond its ecological significance, the plant‐microbiome alliance should be viewed as an emerging opportunity for environmental biotechnology. Plant‐associated microbiomes constitute functional biological platforms capable of providing ecosystem services essential for restoration, including contaminant degradation, nutrient cycling, carbon sequestration and enhanced resilience to environmental stress. Evidence supporting this perspective is emerging across a wide range of restoration contexts. In contaminated soils, plant‐associated microorganisms drive the degradation of hydrocarbons, pesticides, pharmaceuticals and other pollutants through processes collectively known as rhizoremediation (Glick 2010; Kuiper et al. 2004). In post‐mining landscapes, they contribute to nutrient cycling, metal immobilization and soil formation processes, thereby facilitating vegetation establishment (Luo et al. 2023; Mendez and Maier 2008; Zhu et al. 2022). Beneficial microbes also improve drought tolerance and water‐use efficiency in arid environments (De Vries et al. 2018; Liu et al. 2025; Naylor and Coleman‐Derr 2018), while supporting nutrient turnover and carbon sequestration in wetlands and mangrove ecosystems (Alongi 2014; Reef et al. 2010). Although these systems differ substantially in their ecological context, they share a common principle: ecosystem recovery depends just as much on restoring ecological interactions as it does on restoring species. These vital interactions, including plant‐microbe mutualisms, microbial metabolic cooperation and plant–soil feedbacks, are essential to regulate nutrient fluxes, stress responses and overall ecosystem resilience (Berendsen et al. 2012).

4. Engineering Plant‐Microbiome Partnership

As our ability to understand and manipulate these interactions improves, restoration may evolve from the passive recovery of ecological communities to the deliberate deployment of biological functions designed to achieve specific environmental outcomes (Jansson et al. 2023).

This perspective naturally leads to a critical challenge for restoration biotechnology. If microbial communities play a central role in ecosystem recovery, how can they be managed and harnessed to improve restoration outcomes? Early approaches largely relied on microbial inoculants, typically consisting of individual plant growth‐promoting strains (Compant et al. 2019; Molina et al. 2021; Rodriguez‐Conde et al. 2016). While these strategies have provided important proof‐of‐concept studies and, in some cases, successful field applications, they have failed to reproduce the desirable effects due to the complexity and stability of natural microbiomes (Kaminsky et al. 2019). In natural ecosystems, key functions emerge not from individual microorganisms but from interactions among diverse microbial populations, host plants and environmental factors (Molina et al. 2026; Siciliano et al. 2001). Consequently, single‐strain inoculants rarely capture the ecological complexity and functional redundancy that underpin ecosystem resilience (Fitzpatrick et al. 2020).

Promising approaches are emerging from advances in synthetic ecology and microbiome engineering. Rather than focusing on isolated microorganisms, researchers are designing microbial consortia that combine complementary ecological functions. Such communities may integrate pollutant degraders, nitrogen‐fixing bacteria, phosphorus‐solubilizing microorganisms, stress‐protective endophytes and organisms involved in soil aggregation or carbon stabilization. By incorporating both ecological complementarity and functional redundancy, these synthetic microbiomes may provide greater stability and performance under field conditions than conventional inoculants (Han and Yoshikuni 2022; Niu et al. 2017; Sharma 2026; Vorholt et al. 2017).

The convergence of multi‐omics technologies and artificial intelligence may represent one of the most transformative advances in restoration biotechnology. Metagenomics has revealed the extraordinary diversity of environmental microbiomes, while metatranscriptomics, metaproteomics and metabolomics enable the identification of active populations and the functions they perform (Jansson and Hofmockel 2018; Molina et al. 2026; Robinson et al. 2023). However, the direct application of multi‐omics to contaminated soils is not straightforward. Matrices enriched with heavy metals, hydrocarbons, or humic substances frequently hinder DNA, RNA, and protein extraction, resulting in low yields and poor sequencing performance. In addition, stress conditions can accelerate the degradation of environmental mRNA and proteins and induce rapid changes in gene expression patterns. Furthermore, many transcripts, proteins and metabolites cannot be reliably assigned to specific metabolic functions because of incomplete reference databases. Moreover, numerous ecologically relevant molecules occur at very low concentrations, making their detection and quantification challenging. Together, these limitations can introduce biases and provide only an incomplete snapshot of actual microbial activity in contaminated soils (Jansson and Hofmockel 2018; Tartaglia et al. 2020; Peng et al. 2024; Teklay 2026).

Despite these challenges, when integrated with machine‐learning approaches, multi‐omics datasets are opening the door to predictive restoration frameworks capable of identifying optimal plant‐microbiome combinations, forecasting microbiome stability and guiding the design of restoration strategies adapted to specific environmental conditions (Berruto and Demirer 2024; Yu et al. 2026).

The growing enthusiasm surrounding multi‐omics and artificial intelligence should also be approached with caution. Although these technologies have revolutionized our capacity to describe microbiomes and predict ecological interactions, restoration ecology ultimately remains an experimental science. Successful ecosystem recovery cannot be inferred solely from large datasets or computational models, but also requires rigorous validation through cultivation, physiological studies, controlled experiments and field‐scale assessments. In many cases, the ecological relevance of predicted microbial functions remains uncertain until confirmed under realistic environmental conditions. Consequently, future progress will likely depend on combining the predictive power of omics and AI with the mechanistic understanding provided by classical ecological and microbiological approaches (Prosser 2015).

An equally important frontier lies in the integration of plant genetics and microbiome science. Plants actively shape microbiome assembly through root exudates, immune signalling pathways and physiological traits (Fitzpatrick et al. 2020; Trivedi et al. 2020). Consequently, different plant genotypes may recruit microbial communities with distinct functional capacities. Future restoration programs may therefore select plant‐microbiome combinations rather than plant genotypes alone, optimizing both partners to maximize ecosystem recovery (Oyserman et al. 2018, 2022).

5. Holobiont Engineering for Ecosystem Restoration

Building on these advances, we propose Holobiont Engineering for Ecosystem Restoration (HEER) as a conceptual framework for the next generation of restoration biotechnology. Unlike conventional restoration approaches, which primarily focus on species reintroduction and community assembly, HEER treats the plant and its microbiome as a single functional unit. Its goal is not only to recover biodiversity but also to restore ecosystem functions through the deliberate management of plant‐microbiome interactions. By integrating microbiome science, synthetic ecology, multi‐omics technologies, artificial intelligence and ecological theory, this framework seeks to design, monitor and optimize plant‐microbiome partnerships capable of delivering specific restoration outcomes. In this context, ecological interactions become explicit restoration targets rather than passive consequences of ecosystem recovery.

In this context, plants and their microbiomes represent not only ecological partners but also programmable resources for ecosystem engineering.

6. Conclusion

Recent developments suggest that restoration biology is entering a new phase. Rather than relying exclusively on natural assembly processes, restoration may increasingly involve the design, management and optimization of plant‐microbiome systems to accelerate ecosystem recovery. The future of restoration ecology may ultimately depend on a simple but transformative idea: ecosystems recover when relationships recover. Harnessing the plant‐microbe alliance offers an opportunity not only to repair degraded environments, but also to redefine restoration as the deliberate management of ecological partnerships. While multi‐omics and artificial intelligence are expanding our ability to explore and predict these interactions, their real value will ultimately be determined by how effectively they guide experimental discovery and field‐scale restoration. The next generation of restoration strategies will therefore require a close dialogue between computational prediction and ecological validation. In this endeavour, microbial biotechnology has a central role to play in the transition from species‐centred restoration to function‐centred ecosystem recovery.

Author Contributions

Lázaro Molina: conceptualization, writing – original draft, writing – review and editing, supervision. Lucía González‐Pagán: writing – original draft. Ana Segura: conceptualization, writing – original draft, writing – review and editing.

Funding

The authors have nothing to report.

Conflicts of Interest

The authors declare no conflicts of interest.

Data Availability Statement

Data sharing is not applicable to this article as no new data were created or analysed in this study. All data discussed are derived from publicly available sources cited in the references.