Enhancing Microbial Pollutant Degradation by Integrating Eco-Evolutionary Principles with Environmental Biotechnology

We advocate to shift research efforts in environmental biotechnology from searching for desired traits of monocultures that microbial communities. As these will be hard identify with classical genome mining approaches, we recommend using artificial community selection as a tool and select novel and/or enhanced functions.Bioremediation biodegradation artificially selected communities harbors great potential become fast, cost-effective, eco-friendly, socially acceptable way remove pollutants without prior knowledge the involved species degradation pathways needed.The use highly integrated multispecies instead processes result more stable productive cultures.The novelty our proposed approach lies combination eco-evolutionary principles applied biotechnology. This stimulate new advancements biotechnology, likely discovery metabolic pathways. Environmental accumulation anthropogenic is pressing global issue. The by microbes an emerging field but hampered inefficient rates limited enzymes Here, view significant progress can achieved harnessing biological process, makes principles. either directly used bioremediation applications or further analyzed modified, instance through systems biology, synthetic genetic engineering. then inform machine learning enhance Pollution, atmosphere, soil, water, serious challenge 21st century. Deleterious impacts on aquatic ecosystems are triggered different sources pollution including sewage, nutrients terrigenous materials, crude oil, heavy metals, plastics [1.Häder D.-P. et al.Anthropogenic ecosystems: problems implications.Sci. Total Environ. 2020; 713: 136586Crossref PubMed Scopus (138) Google Scholar]. Importantly, oceans comprise largest biome planet operate sink many pollutants, such plastics. It estimated 80% plastic ocean comes land-based reaches via rivers wastewater treatment facilities [2.Amaral-Zettler L.A. al.Ecology plastisphere.Nat. Rev. Microbiol. 18: 139-151Crossref (242) In 2010, it was 5–13 million tons entered [3.Jambeck J.R. al.Plastic waste inputs land into ocean.Science. 2015; 347: 768-771Crossref (4638) Scholar], where they accumulate various habitats, marine sediments, ingestion at trophic levels food web. Many concern because significantly affect human ecosystem health around world, instance, contaminants (CECs) [4.Nilsen E. al.Critical review: grand challenges assessing adverse effects webs.Environ. Toxicol. Chem. 2018; 38: 46-60Crossref (70) persistent organic (POPs) [5.Jamieson A.J. al.Bioaccumulation deepest fauna.Nat. Ecol. Evol. 2017; 1: 51Crossref (168) endocrine disrupting chemicals (EDCs) [6.Zhou X. al.Endocrine wild freshwater fishes: species, tissues, sizes, risks.Environ. Pollut. 244: 462-468Crossref (46) Therefore, restoration conservation future generations should utmost priority. To date, remediation techniques, physical, chemical, biological, have been removal contaminants. Despite fact physical chemical approaches practiced decades, still suffer several drawbacks. These include high processing costs, increased requirements reagents, undesirable generation secondary [7.Dangi A.K. al.Bioremediation microbes: biology engineering approach.Crit. Biotechnol. 39: 79-98Crossref (90) By contrast, (bioremediation, see Glossary) form microbe-based treatments, metals [8.Iravani S. Varma R.S. Bacteria metal nanoparticle biosynthesis.ACS Sustain. Eng. 8: 5395-5409Crossref (42) pesticides [9.Rodríguez A. al.Omics pesticide biodegradation.Curr. 77: 545-563Crossref (34) hydrocarbons [10.Ławniczak Ł. al.Microbial - basic bioremediation: review.Molecules. 25: 856Crossref (77) Scholar] environment. Nevertheless, while culturable bacteria were isolated contaminated sites already 45 years ago [11.Raymond R.L. al.Final Report Beneficial Stimulation Bacterial Activity Ground Waters Containing Petroleum Products. American Institute (API), Committee Affairs, Sun Ventures Inc., 1975Google has so far failed provide convincible solutions pollutant management. Classically, majority studies performed aimed isolate, culture, characterize organisms responsible process [12.Head I.M. al.Bioremediation: critical review. Horizon Scientific Press, 2003Google While culture-based techniques resulted identification number carrying out specific (Malla al. [13.Malla M.A. al.Understanding designing strategies microbe-mediated omics approaches.Front. 9: 1132Crossref (101) examples), suffers important One than 99% microorganisms exist environment cannot cultivated (easily) under laboratory conditions. This, known ‘great plate count anomaly’ [14.Staley J.T. Konopka Measurement situ activities nonphotosynthetic terrestrial habitats.Annu. 1985; 321-346Crossref (920) made recovery isolates for, participate in, given challenging. so-called recalcitrant microplastics POPs, particularly problematic slow due lack efficient [15.Janssen D.B. al.Bacterial xenobiotic compounds: evolution distribution enzyme activities.Environ. 2005; 7: 1868-1882Crossref (171) exemplified non-native polymer polyethylene terephthalate (PET), sixth most produced Europe. Even though PET one best understood mechanisms only mere handful verified active degrade discovered bacterial fungal strains [16.Yoshida al.A bacterium degrades assimilates poly (ethylene terephthalate).Science. 2016; 351: 1196-1199Crossref (873) Scholar, 17.Müller R.-J. al.Enzymatic poly(ethylene terephthalate): rapid hydrolyse hydrolase T. fusca.Macromol. Rapid Commun. 26: 1400-1405Crossref (237) 18.Danso D. al.Plastics: biotechnological perspectives degradation.Appl. 2019; 85: 768-14Crossref (181) application their comparatively low conversion do not suffice industrial application. A current focus therefore search enzymes, well improvement existing ones, example, rational protein [19.Son H.F. al.Rational thermo-stable PETase Ideonella sakaiensis degradation.ACS Catal. 3519-3526Crossref (107) bioinformatically-aided mutagenesis [20.Tournier V. al.An engineered depolymerase break down recycle bottles.Nature. 580: 216-219Crossref (329) With advancement recombinant DNA technologies, rejuvenated allowed creation whole hosting genes efficiencies (Box 1). rely genetically organisms. understand Earth’s ecosystems, specifically if interact indigenous during thus pose danger results strict containment protocols administrative restrictions field. Further, despite recent advances meta-omics (e.g., genomics, transcriptomics, proteomics, metabolomics) generated data improving understanding cellular processes, control, signaling networks [21.Zhang al.Advancing functional translational microbiome approaches.Microbiome. 154Crossref (74) detailed enzymes. linking function experimentally showcased Quistad [22.Quistad S.D. al.Experimental manipulation selfish elements links function.Philos. Trans. R. Soc. B. 375: 20190681Crossref (7) regularly added replicate particular regime (i.e., nitrogen-limited conditions). Over course 48-week-long experiment, movement enrichment ecologically genes, which mainly nitrogen metabolism, could detected within comparative metagenomics.Box 1Recombinant Technologies BioremediationGenetic enables higher Scholar,20.Tournier Scholar,64.Basu al.Engineering PGPMOs gene editing biology: solution phytoremediation?.Trends 36: 499-510Abstract Full Text PDF (41) Tools like rational/semirational design [65.Korendovych I.V. Rational semirational design.in: Bornscheuer U. Höhne M. Protein Engineering. Methods Molecular Biology. vol 1685. Humana 2018: 15-23Google directed [66.Porter J.L. al.Directed biocatalysis.ChemBioChem. 17: 197-203Crossref (131) fast-evolving fields incorporated [67.Li G. al.Can revolutionize selective enzymes?.Adv. Synth. 361: 2377-2386Google towards optimizing biocatalysts tasks, increasing enantioselectivity, robustness respect solvents, temperature. Besides optimization, transform biocatalytic perform functions create multifunctional [68.Alonso al.Genetically proteins two biocatalysis synergistic chemo-and biocatalysis.Nat. 3: 319-328Crossref cascades, capable combining enzymatic activity ‘biological factories’ [69.Zhang Y. Hess H. Toward high-efficiency cascades.ACS 6018-6027Crossref comprehensive overview purposes available Scholar,70.Sanghvi al.Engineered bioremediation.in: Pandey V.C. Singh Bioremediation Pollutants. Elsevier, 2020: 359-374Crossref Scholar].Another promising transfer metagenomic [71.Sheth R.U. al.Manipulating engineering.Trends Genet. 32: 189-200Abstract (119) accelerated applying RNA-targeting CRISPR system [72.Smargon A.A. al.RNA-targeting transcriptomic engineering.Nat. Cell Biol. 22: 143-150Crossref (26) method mouse gut [73.Ronda C. al.Metagenomic mammalian situ.Nat. Methods. 16: 167-170Crossref (79) shown Escherichia coli deliver payloads original sustainable way. underlying principle involves desirable spread throughout community. vertically horizontally transmitted native microbiomes need large perturbations stressors, antibiotics. integration iterative design-build-test-learn (DBTL) cycle, phytoremediation Basu [64.Basu Lawson [74.Lawson C.E. al.Common practices microbiomes.Nat. 725-741Crossref (129) ideal timely accelerates both scientific translation innovative solutions. Genetic Another this opinion article, implement bioremediation, integrate believe implementing speed up discovering relevant pathways, no needed. relies unexplored diversity reside ecosystems. Microorganisms usually single, identical strains, live together other taxonomically metabolically diverse [23.Zelezniak al.Metabolic dependencies drive co-occurrence communities.Proc. Natl. Acad. Sci. 112: 6449-6454Crossref (331) Such characterized spatial structure, provides vicinity interactions between its members, exchange metabolites [24.Nadell C.D. al.Spatial cooperation, competition biofilms.Nat. 14: 589-600Crossref (408) offer advantages know macroecological surveys across there positive relationships biodiversity functioning. high-diversity mixtures found compared equivalent [25.Tilman al.Biodiversity functioning.Annu. Syst. 2014; 45: 471-493Crossref (835) included study, same relationship expected parameters productivity), reasons why (at genotype level) probably productive, includes ability utilize resources efficiently when monocultures, initially all cells metabolize substrate. resource utilization refers readily external environment, released fellow members [26.Gravel niche alters strength diversity-productivity relationship.Nature. 2010; 469: 89-92Crossref (133) Comparative analyses genomes suggest 98% sequenced auxotrophs and, thus, byproducts [27.Zengler K. Zaramela L.S. social network how auxotrophies shape complex communities.Nat. 383-390Crossref (128) comparison robust against ecological disturbances, exposure antibiotics, changes oxygen pH levels, invasion part before, encountering protozoan predators parasites [28.Giri al.Harnessing evolutionary guide production consortia.Curr. Opin. 62: 228-238Crossref (16) Within communities, certain present incredibly abundances. however recognized that, particular, rare biosphere fulfills essential functionality abundant [29.Jousset al.Where less may more: pulls strings.ISME J. 11: 853-862Crossref (428) observations strongly increase [30.Cavaliere al.Cooperation applications.Environ. 19: 2949-2963Crossref (83) key cross-feeding [31.Pande Kost unculturability formation intercellular networks.Trends 349-361Abstract (88) growth survival, entities must coevolved respective often considered suitable purposes, representative situation exists nature. Synergistic facilitate emergence biosynthetic would difficult impossible achieve Scholar,32.Chiu H.-C. al.Emergent capacity simple communities.PLoS Comput. 10e1003695Crossref (62) An area, benefit harnessed wastewater. demonstrated natural microalgae–bacteria consortia lead overall uptake [33.Gonçalves A.L. review microalgal treatment.Algal Res. 24: 403-415Crossref (299) Mathematical modeling burden resulting decrease system’s productivity [34.Tsoi division labor systems.Proc. 115: 2526-2531Crossref (92) result, showing labor, distinct parts population complementary steps pathway, outperform uniform populations compartmentalization reactions increases modularity [35.Tsoi al.Emerging communities.Biotechnol. Adv. 37: 107372Crossref (35) Further consider downstream applications, tend resistant resilient disturbances presented changing conditions, predict breakdown bioprocess based monocultures. All findings emphasize think about individually occurring habitats [36.van Gestel Kolter When stop thinking cells.J. Mol. 431: 2487-2492Crossref (6) easily deconstructed individual components. Instead, appreciated differentiated groups integrated, analogous differentiation observed multicellular Engineering advance biosynthesis bioproduction medicines, biofuels, biomaterials) bioremediation. Synthetic tasks challenging realized Advances allow us control program behavior (synthetic tools reviewed Tsoi Scholar]). consortia, strategy dependent inter-species interest,