Metagenomics is a field of research that focuses on the study of genetic material obtained directly from environmental samples such as soil, water, or even the human gut (Yen and Johnson, 2021). Unlike traditional genomics, which focuses on the DNA of individual organisms, metagenomics examines the collective genetic material of all microorganisms present in a given sample (New and Brito, 2020). The core idea of metagenomics is to analyze the genetic diversity and functional potential of entire microbial communities without the need to isolate and culture individual organisms (Berini et al., 2017). This approach allows us to gain insights into the composition, structure, and functional capabilities of complex microbial ecosystems that are difficult to study using conventional molecular biological methods (Garrido-Cardenas and Manzano-Agugliaro, 2017).

Metagenomics involves sequencing and analyzing the DNA or RNA present in a sample from a particular ecological niche (Marco, 2008). Because this material is normally fragmented and piecemeal, advanced sequencing technologies are used to retrieve genetic information. By analyzing the sequences, it is possible to identify the species of microorganisms present, their relative abundance and the functional genes they carry (Kayani et al., 2021). This information can provide valuable insights into ecosystem dynamics, microbial interactions, and potential applications in biotechnology and environmental research as elaborated in our study. In principle, metagenomics allows us to explore the genetic composition of entire microbial communities in their natural habitats and thus discover the hidden biodiversity and functional potential of these ecosystems (Bouhajja et al., 2016). Here, we describe possible pathways to “synthetic metagenomics” (Figure 1) by merging SynBio with classical metagenomics.

In this context, metagenomics is evolving into a technology that complements gene and protein engineering methods and applies SynBio’s system design concepts (see above). Metagenomics exploits the wealth of genetic and biochemical diversity present in the genomes of microorganisms in environmental samples (Figure 1) and offers a range of new technologies for screening novel catalytic activities from environmental samples with potential biotechnological applications (Guazzaroni et al., 2015) or even diagnostics (Greninger, 2018). For example, metagenomic analyses of marine ecosystems have begun to reveal the extent of novel compounds encoded in the vast bacterial richness and diversity of the marine ecosystem (Tseng and Tang, 2014). A combination of unique physicochemical properties and spatial niche-specific substrates in wide-spread and extreme habitats underscores the potential of the marine environment to deliver functionally novel biocatalytic activities (Parages et al., 2016).

In recent years, metagenomics has expanded our understanding of how the collective functions of microorganisms emerge from the complex web of interactions between their genetic and metabolic potentials and the environment to enable useful applications in terms of environmental sustainability (Sharma et al., 2022). A particular focus of metagenomics is the study of the interactions of environmental pollutants (xenobiotics) of anthropogenic origin (e.g., plastics, pharmaceuticals, pesticides, cosmetics, flavorings, fragrances, food additives, industrial chemicals, and plastics) with the local environment and their global impacts (Danso et al., 2019). Metagenomic analyses have expanded our understanding of ecosystems and biodiversity in several fields such as antimicrobial resistance in waste management systems, bioremediation of oil spills, and biodegradation of plastics.

Therefore, synthetic metagenomics can be seen as an emerging field of research in which metagenomes are studied functionally following the key postulates of SynBio (see above). This approach substantially expands the set of identified biological activities and building blocks. For example, functional metagenomic of metabolic pathways in microbial communities has led to the discovery of novel bioactivities such as amidases, NF-κB modulators, naphthalene degrading enzymes, cellulases, lipases, and transporters (Robinson et al., 2021). Using these genetic devices and circuits as templates along with their further functional integration, improvements can be made by altering or redesigning metabolic pathways in selected microbial chassis to improve synthesis and yield of high-value products (van der Helm et al., 2018).

The emergence and the spread of antimicrobial resistance in animal husbandry is a growing global concern (Karbalaei-Heidari and Budisa, 2020). Metagenomics has proven to be a powerful tool for analyzing the evolution of antimicrobial resistance genes (ARGs) and mobile genetic elements (MGEs) in microbiome of animals. Large quantities of veterinary pharmaceuticals and drugs are used not only to treat infectious diseases, but also as prophylactic therapies and feed enhancers, potentially leading to the selection of ARGs, MGEs, and ultimately, antimicrobial resistance bacteria (ARBs). For instance, the study of the “Resistome” (complete set of ARGs) in ruminal microbiomes has shown the presence of ARGs encoding resistance to tetracyclines, one of the most used antibiotics in farms, in the genomes of common ruminal species (Sabino et al., 2019). Not surprisingly, animal manures are significant reservoir of ARGs and MGEs and can promote the development of ARBs, which are often spread in agricultural fields when manure is applied as fertilizer (Buta-Hubeny et al., 2022).

In this context, metagenomics and microbial diversity analyses provide a valuable framework for studying the impact of different manure treatments on resistomes and mobilomes (complete set of MGEs). Through these technologies, we are gaining a better understanding of the microbial species that harbor antimicrobial resistant elements and the dynamics that drive changes in ARGs and MGEs. For example, metagenomic analyses have shown that microbial successions during the mesophilic and thermophilic stages of manure composting or the establishment of anaerobic consortia during anaerobic digestion (AD), can reduce the abundance and diversity of ARGs and MGEs in animal manure (Cheng, 2017; Flores-Orozco et al., 2023; Flores-Orozco et al., 2023). The knowledge gained from these applications is crucial for addressing the serious health problem that antimicrobial resistance poses and for developing strategies to minimize the risk of its spread in agriculture.

Advances in microbial genetics and “omics” techniques have facilitated the analysis of microbial communities beyond the limited reach of conventional culturing methods, which generally focus on the growth and activity of single organisms under optimal laboratory conditions. Metagenomics has expanded scientific knowledge of complex microbial communities, enabling analysis of interactions among microbes in the community, as well as co-metabolism, enzyme activity, and biodegradation of oil in the natural environment. “Omics” tools, such as metagenomics and meta-transcriptomics give researchers and spill responders the ability to assess the biodegradation capacity of the native microbial community at a spill site and provide them with further information on whether and to what extent further action is needed (Czaplicki and Gunsch, 2016; Ghosal et al., 2016; Techtmann and Hazen, 2016; Mukherjee et al., 2017).

Oil is a naturally occurring, non-renewable energy source that can cause severe detrimental environmental damage if released in large quantities, such as in an accidental spill. Crude oil is a mixture of thousands of compounds, of which polycyclic aromatic compounds (PACs) are of particular concern due to their acute and chronic toxicity, mutagenicity, and carcinogenicity to interacting organisms (Cao et al., 2009; Dupuis and Ucan-Marin, 2015). PACs consist of two or more fused benzene rings and vary in structure, complexity, and recalcitrance (Haritash and Kaushik, 2009; Lee, 2015). The larger the compound, the more persistent it is likely to be in the environment (Rosenberg and Ron, 1996). To limit the impact of oil on habitats, biota, and nearby communities, mechanical and chemical measures are commonly used in oil spills to facilitate removal or degradation of the oil. However, some of these conventional methods are invasive and cause damage to sensitive habitats and leave oil behind (Zhu et al., 2001). Increasing research and attention has been given to non-invasive alternatives in which native microorganisms play a role in removing oil compounds from the environment after an oil spill (Ghosal, Ghosh, Dutta and Ahn, 2016).

The potential of bioremediation to fill the sustainability gap is substantial when guided by the right insights. The refinement of bioremediation practices can be achieved through the integration of novel “OMICS” methodologies aimed at deciphering the microbiome associated with hydrocarbon plastics. To attain this objective, an exhaustive understanding of bacterial and fungal degradation pathways, their intricate interplays within microbiomes, and their interactions with the soil matrix is imperative. Leveraging “OMICS” techniques facilitates the investigation of both cultivable and non-cultivable soil microbial communities engaged in degradation processes, offering tools to pinpoint pivotal organisms responsible for degrading soil pollutants and reinstating soil vitality and resilience. To do this, we need to thoroughly investigate microbial communities, their degradation pathways, and their complex interactions. Numerous studies provided detailed explanations of genomic and metagenomic methods, as well as the tools necessary to decipher the information obtained. These methods are applicable in two ways: first, to refine bio-based strategies for effectively treating soils contaminated by petroleum hydrocarbons, and second, to facilitate the smooth up-scaling of these technologies to industrial scales (Chicca et al., 2022; Chicca et al., 2022; Becarelli et al., 2023).

Petroleum-based synthetic plastics such as polyethylene (PE), polypropylene (PP), polyvinylchloride (PVC), polyethylene terephthalate (PET), and polystyrene (PS) are the indispensable components of modern industry and daily life but have caused significant environmental problems world-wide due to their extreme recalcitrance to biodegradation in the environments (Krueger et al., 2015; MacLeod et al., 2021). Since current management strategies such as landfills, incineration, and mechanical recycling, are not sufficient to cope with the increasing amount of plastic waste (Drzyzga and Prieto, 2019; Lim and San Thian, 2022; Ackerman and Levin, 2023), biodegradation of these plastics and biotechnological recycling have emerged as an alternative and become one of the research areas actively studied worldwide. Several studies also showed that certain microbial groups have been enriched in plastic films or microplastics in terrestrial environments. Chung et al. (2022) compared the microbial communities on the plastic waste films, which were mostly made of PE and had been buried in the four landfill sites for more than 20 years, with those in the nearby soils assuming that specific and plastic-degrading microorganisms were enriched on the WPFs. The Fourier-transform infrared (FTIR) spectroscopy showed that the WPFs were oxidized, though not as much as when exposed to UV-light and oxygen.

Microbial communities were primarily characterized by their geographical origins, but communities on WPFs generally had lower species richness and diversity than those in nearby soils and exhibited community structures that differed from those in nearby soils. The species taxonomically close to Bradyrhizobiaceae, Pseudarthrobacter (formerly known as Arthrobacter), and Bacillus in the bacterial communities and the one close to Mortierella in the fungal communities were enriched on the WPFs, suggesting that they might be involved in the degradation of the plastic waste films. The network analysis also indicated that the species related to Mortierella was one of the keystone species on the WPFs. Several studies reported that Arthrobacter and Mortierella were also enriched on plastics in soils (Gao et al., 2021; Wright et al., 2021; Yi et al., 2021) or had the ability to degrade plastics (Albertsson et al., 1998; Han et al., 2020). For example, metagenomic analyses have shown that specific and common microbial groups adapt to plastics in terrestrial and marine environments. While there is not yet direct evidence that these microbes are directly responsible for degrading plastics is not yet available, SynBio technologies may soon confirm this hypothesis.