MICROBIOME STUDIES FROM SAUDI ARABIA OVER THE LAST 10 YEARS: ACHIEVEMENTS, GAPS, AND FUTURE DIRECTIONS

Main Article Content

Albanaqi, Alsaeedi Lafi A, Alhazmi, Abdullah Ashi S, Albanaqi Riyadh Mohammed R, Salman Solaiman Mosleh Aloufi., Mohammed Saud Mubarak Alotaibi, Mohammed Ali Abdulrahman Alabdulmunim, Abdullah Ibrahim Mohammed Alzhrani

Keywords

microbiome, metagenome, health, environment, surveillance, novel bioactive compounds, antimicrobial resistance, food processing, novel strains, space biology, Saudi Arabia

Abstract

Over the last decade, research on the microbiome has demonstrated significant promise in terms of advancing our comprehension of the structures and functions of microbiomes in diverse biomes and harnessing this knowledge for the benefit of humanity. Geographical, ecological, ethnic, industrial, and scientific capabilities abound in Saudi Arabia. As a result, Saudi Arabia possesses considerable capacity to conduct and implement applications and research pertaining to the microbiome. Nevertheless, an analysis of Saudi Arabia's position in relation to worldwide trends in microbiome research is currently unavailable. This article compares the research on the metagenome-assisted microbiome conducted in Saudi Arabia to the worldwide emphasis on microbiome studies. Additionally, it underscores the deficiencies and domains that warrant the attention of microbiome researchers in Saudi Arabia, as well as potential endeavours that the Saudi government and universities could undertake. The literature review demonstrates that worldwide microbiome research trends encompass a wide range of topics, including surveillance of antimicrobial resistance and environmental and animal health conditions and diseases, investigation of food and food processing, development of innovative industrial enzymes and bioactive pharmaceutical products, and applications in space. In contrast, over the past decade, Saudi microbiome research has been largely inapplicable and restricted to a small number of health (human and animal) and environmental/ecological aspects. In order to align with global trends, Saudi Arabia should increase its emphasis on applied microbiome research via initiatives from the government, academia, and industry, as well as international cooperation.

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1. Berg G., Rybakova D., Fischer D., Cernava T., Vergès M.-C.C., Charles T., Chen X., Cocolin L., Eversole K., Corral G.H., et al. Microbiome definition re-visited: Old concepts and new challenges. Microbiome. 2020;8:103. doi: 10.1186/s40168-020-00875-0. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 2. Cullen C.M., Aneja K.K., Beyhan S., Cho C.E., Woloszynek S., Convertino M., McCoy S.J., Zhang Y., Anderson M.Z., Alvarez-Ponce D., et al. Emerging Priorities for Microbiome Research. Front. Microbiol. 2020;11:136. doi: 10.3389/fmicb.2020.00136. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 3. Kumar Awasthi M., Ravindran B., Sarsaiya S., Chen H., Wainaina S., Singh E., Liu T., Kumar S., Pandey A., Singh L., et al. Metagenomics for taxonomy profiling: Tools and approaches. Bioengineered. 2020;11:356–374. doi: 10.1080/21655979.2020.1736238. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 4. Roumpeka D.D., Wallace R.J., Escalettes F., Fotheringham I., Watson M. A Review of Bioinformatics Tools for Bio-Prospecting from Metagenomic Sequence Data. Front. Genet. 2017;8:23. doi: 10.3389/fgene.2017.00023. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 5. Escobar-Zepeda A., Godoy-Lozano E.E., Raggi L., Segovia L., Merino E., Gutiérrez-Rios R.M., Juarez K., Licea-Navarro A.F., Pardo-Lopez L., Sanchez-Flores A. Analysis of sequencing strategies and tools for taxonomic annotation: Defining standards for progressive metagenomics. Sci. Rep. 2018;8:12034. doi: 10.1038/s41598-018-30515-5. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 6. Hasanean H., Almazroui M. Rainfall: Features and Variations over Saudi Arabia, A Review. Climate. 2015;3:578–626. doi: 10.3390/cli3030578. [CrossRef] [Google Scholar] 7. Al-Obaid S., Samraoui B., Thomas J., El-Serehy H.A., Alfarhan A.H., Schneider W., O’Connell M. An overview of wetlands of Saudi Arabia: Values, threats, and perspectives. Ambio. 2016;46:98–108. doi: 10.1007/s13280-016-0807-4. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 8. Herzallah H.K., Antonisamy B.R., Shafee M.H., Al-Otaibi S.T. Temporal trends in the incidence and demographics of cancers, communicable diseases, and non-communicable diseases in Saudi Arabia over the last decade. Saudi Med. J. 2019;40:277–286. doi: 10.15537/smj.2019.3.23585. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 9. Al-Hanawi M.K., Keetile M. Socio-Economic and Demographic Correlates of Non-communicable Disease Risk Factors Among Adults in Saudi Arabia. Front. Med. 2021;8:605912. doi: 10.3389/fmed.2021.605912. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 10. Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214. doi: 10.1038/nature11234. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 11. Gaulke C.A., Sharpton T.J. The influence of ethnicity and geography on human gut microbiome composition. Nat. Med. 2018;24:1495–1496. doi: 10.1038/s41591-018-0210-8. [PubMed] [CrossRef] [Google Scholar] 12. Premaraj T.S., Vella R., Chung J., Lin Q., Panier H., Underwood K., Premaraj S., Zhou Y. Ethnic variation of oral microbiota in children. Sci. Rep. 2020;10:14788. doi: 10.1038/s41598-020-71422-y. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 13. Wilson A.S., Koller K.R., Ramaboli M.C., Nesengani L.T., Ocvirk S., Chen C., Flanagan C.A., Sapp F.R., Merritt Z.T., Bhatti F., et al. Diet and the Human Gut Microbiome: An International Review. Dig. Dis. Sci. 2020;65:723–740. doi: 10.1007/s10620-020-06112-w. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 14. Chen Y., Zhou J., Wang L. Role and Mechanism of Gut Microbiota in Human Disease. Front. Cell. Infect. Microbiol. 2021;11:625913. doi: 10.3389/fcimb.2021.625913. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 15. Willis J.R., Gabaldón T. The Human Oral Microbiome in Health and Disease: From Sequences to Ecosystems. Microorganisms. 2020;8:308. doi: 10.3390/microorganisms8020308. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 16. Anahtar M.N., Gootenberg D.B., Mitchell C.M., Kwon D.S. Cervicovaginal Microbiota and Reproductive Health: The Virtue of Simplicity. Cell Host Microbe. 2018;23:159–168. doi: 10.1016/j.chom.2018.01.013. [PubMed] [CrossRef] [Google Scholar] 17. Chen X., Lu Y., Chen T., Li R. The Female Vaginal Microbiome in Health and Bacterial Vaginosis. Front. Cell. Infect. Microbiol. 2021;11:631972. doi: 10.3389/fcimb.2021.631972. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 18. Khare R., Espy M.J., Cebelinski E., Boxrud D., Sloan L.M., Cunningham S.A., Pritt B.S., Patel R., Binnicker M.J. Comparative evaluation of two commercial multiplex panels for detection of gastrointestinal pathogens by use of clinical stool specimens. J. Clin. Microbiol. 2014;52:3667–3673. doi: 10.1128/JCM.01637-14. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 19. Leber A.L., Everhart K., Balada-Llasat J.-M., Cullison J., Daly J., Holt S., Lephart P., Salimnia H., Schreckenberger P.C., DesJarlais S., et al. Multicenter Evaluation of BioFire FilmArray Meningitis/Encephalitis Panel for Detection of Bacteria, Viruses, and Yeast in Cerebrospinal Fluid Specimens. J. Clin. Microbiol. 2016;54:2251–2261. doi: 10.1128/JCM.00730-16. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 20. Ruggiero P., McMillen T., Tang Y.-W., Babady N.E. Evaluation of the BioFire FilmArray respiratory panel and the GenMark eSensor respiratory viral panel on lower respiratory tract specimens. J. Clin. Microbiol. 2014;52:288–290. doi: 10.1128/JCM.02787-13. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 21. Tang Y.-W., Gonsalves S., Sun J.Y., Stiles J., Gilhuley K.A., Mikhlina A., Dunbar S.A., Babady N.E., Zhang H. Clinical Evaluation of the Luminex NxTAG Respiratory Pathogen Panel. J. Clin. Microbiol. 2016;54:1912–1914. doi: 10.1128/JCM.00482-16. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 22. Schlaberg R., Queen K., Simmon K., Tardif K., Stockmann C., Flygare S., Kennedy B., Voelkerding K., Bramley A., Zhang J., et al. Viral Pathogen Detection by Metagenomics and Pan-Viral Group Polymerase Chain Reaction in Children with Pneumonia Lacking Identifiable Etiology. J. Infect. Dis. 2017;215:1407–1415. doi: 10.1093/infdis/jix148. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 23. Blauwkamp T.A., Thair S., Rosen M.J., Blair L., Lindner M.S., Vilfan I.D., Kawli T., Christians F.C., Venkatasubrahmanyam S., Wall G.D., et al. Analytical and clinical validation of a microbial cell-free DNA sequencing test for infectious disease. Nat. Microbiol. 2019;4:663–674. doi: 10.1038/s41564-018-0349-6. [PubMed] [CrossRef] [Google Scholar] 24. Miller S., Naccache S.N., Samayoa E., Messacar K., Arevalo S., Federman S., Stryke D., Pham E., Fung B., Bolosky W.J., et al. Laboratory validation of a clinical metagenomic sequencing assay for pathogen detection in cerebrospinal fluid. Genome Res. 2019;29:831–842. doi: 10.1101/gr.238170.118. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 25. Wong A.C., Levy M. New Approaches to Microbiome-Based Therapies. mSystems. 2019;4:e00122-19. doi: 10.1128/mSystems.00122-19. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 26. Barrientos-Durán A., Fuentes-López A., de Salazar A., Plaza-Díaz J., García F. Reviewing the Composition of Vaginal Microbiota: Inclusion of Nutrition and Probiotic Factors in the Maintenance of Eubiosis. Nutrients. 2020;12:419. doi: 10.3390/nu12020419. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 27. Sun Y., Baptista L.C., Roberts L.M., Jumbo-Lucioni P., McMahon L.L., Buford T.W., Carter C.S. The Gut Microbiome as a Therapeutic Target for Cognitive Impairment. J. Gerontol. A Biol. Sci. Med. Sci. 2020;75:1242–1250. doi: 10.1093/gerona/glz281. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 28. Mueller U.G., Sachs J.L. Engineering Microbiomes to Improve Plant and Animal Health. Trends Microbiol. 2015;23:606–617. doi: 10.1016/j.tim.2015.07.009. [PubMed] [CrossRef] [Google Scholar] 29. Peixoto R.S., Harkins D.M., Nelson K.E. Advances in Microbiome Research for Animal Health. Annu. Rev. Anim. Biosci. 2021;9:289–311. doi: 10.1146/annurev-animal-091020-075907. [PubMed] [CrossRef] [Google Scholar] 30. Garlapati D., Charankumar B., Ramu K., Madeswaran P., Ramana Murthy M.V. A review on the applications and recent advances in environmental DNA (eDNA) metagenomics. Rev. Environ. Sci. Biotechnol. 2019;18:389–411. doi: 10.1007/s11157-019-09501-4. [CrossRef] [Google Scholar] 31. Karsenti E., Acinas S.G., Bork P., Bowler C., De Vargas C., Raes J., Sullivan M., Arendt D., Benzoni F., Claverie J.-M., et al. Tara Oceans Consortium. A holistic approach to marine eco-systems biology. PLoS Biol. 2011;9:e1001177. doi: 10.1371/journal.pbio.1001177. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 32. Gorsky G., Bourdin G., Lombard F., Pedrotti M.L., Audrain S., Bin N., Boss E., Bowler C., Cassar N., Caudan L., et al. Expanding Tara Oceans Protocols for Underway, Ecosystemic Sampling of the Ocean-Atmosphere Interface During Tara Pacific Expedition (2016–2018) Front. Mar. Sci. 2019;6:750. doi: 10.3389/fmars.2019.00750. [CrossRef] [Google Scholar] 33. Lax S., Smith D.P., Hampton-Marcell J., Owens S.M., Handley K.M., Scott N.M., Gibbons S.M., Larsen P., Shogan B.D., Weiss S., et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048–1052. doi: 10.1126/science.1254529. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 34. Gibbons S.M., Jones E., Bearquiver A., Blackwolf F., Roundstone W., Scott N., Hooker J., Madsen R., Coleman M.L., Gilbert J.A. Human and environmental impacts on river sediment microbial communities. PLoS ONE. 2014;9:e97435. doi: 10.1371/journal.pone.0097435. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 35. Espínola F., Dionisi H.M., Borglin S., Brislawn C.J., Jansson J.K., Mac Cormack W.P., Carroll J., Sjöling S., Lozada M. Metagenomic Analysis of Subtidal Sediments from Polar and Subpolar Coastal Environments Highlights the Relevance of Anaerobic Hydrocarbon Degradation Processes. Microb. Ecol. 2018;75:123–139. doi: 10.1007/s00248-017-1028-5. [PubMed] [CrossRef] [Google Scholar] 36. Techtmann S.M., Hazen T.C. Metagenomic applications in environmental monitoring and bioremediation. J. Ind. Microbiol. Biotechnol. 2016;43:1345–1354. doi: 10.1007/s10295-016-1809-8. [PubMed] [CrossRef] [Google Scholar] 37. Köchling T., Sanz J.L., Galdino L., Florencio L., Kato M.T. Impact of pollution on the microbial diversity of a tropical river in an urbanized region of northeastern Brazil. Int. Microbiol. 2017;20:11–24. doi: 10.2436/20.1501.01.281. [PubMed] [CrossRef] [Google Scholar] 38. Imchen M., Kumavath R., Barh D., Vaz A., Góes-Neto A., Tiwari S., Ghosh P., Wattam A.R., Azevedo V. Comparative mangrove metagenome reveals global prevalence of heavy metals and antibiotic resistome across different ecosystems. Sci. Rep. 2018;8:11187. doi: 10.1038/s41598-018-29521-4. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 39. Zhuang M., Sanganyado E., Li P., Liu W. Distribution of microbial communities in metal-contaminated nearshore sediment from Eastern Guangdong, China. Environ. Pollut. 2019;250:482–492. doi: 10.1016/j.envpol.2019.04.041. [PubMed] [CrossRef] [Google Scholar] 40. Acinas S.G., Sánchez P., Salazar G., Cornejo-Castillo F.M., Sebastián M., Logares R., Royo-Llonch M., Paoli L., Sunagawa S., Hingamp P., et al. Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities. Commun. Biol. 2021;4:604. doi: 10.1038/s42003-021-02112-2. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 41. Bourhane Z., Lanzén A., Cagnon C., Said O.B., Mahmoudi E., Coulon F., Atai E., Borja A., Cravo-Laureau C., Duran R. Microbial diversity alteration reveals biomarkers of contamination in soil-river-lake continuum. J. Hazard. Mater. 2021;421:126789. doi: 10.1016/j.jhazmat.2021.126789. [PubMed] [CrossRef] [Google Scholar] 42. Wang Y., Liao S., Gai Y., Liu G., Jin T., Liu H., Gram L., Strube M.L., Fan G., Sahu S.K., et al. Metagenomic Analysis Reveals Microbial Community Structure and Metabolic Potential for Nitrogen Acquisition in the Oligotrophic Surface Water of the Indian Ocean. Front. Microbiol. 2021;12:518865. doi: 10.3389/fmicb.2021.518865. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 43. Suttner B., Johnston E.R., Orellana L.H., Rodriguez-R L.M., Hatt J.K., Carychao D., Carter M.Q., Cooley M.B., Konstantinidis K.T. Metagenomics as a Public Health Risk Assessment Tool in a Study of Natural Creek Sediments Influenced by Agricultural and Livestock Runoff: Potential and Limitations. Appl. Environ. Microbiol. 2020;86:e02525-19. doi: 10.1128/AEM.02525-19. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 44. Hendriksen R.S., Munk P., Njage P., van Bunnik B., McNally L., Lukjancenko O., Röder T., Nieuwenhuijse D., Pedersen S.K., Kjeldgaard J., et al. Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nat. Commun. 2019;10:1124. doi: 10.1038/s41467-019-08853-3. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 45. Yadav S., Kapley A. Antibiotic resistance: Global health crisis and metagenomics. Biotechnol. Rep. 2021;29:e00604. doi: 10.1016/j.btre.2021.e00604. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 46. Filipic B., Novovic K., Studholme D.J., Malesevic M., Mirkovic N., Kojic M., Jovcic B. Shotgun metagenomics reveals differences in antibiotic resistance genes among bacterial communities in Western Balkans glacial lakes sediments. J. Water Health. 2020;18:383–397. doi: 10.2166/wh.2020.227. [PubMed] [CrossRef] [Google Scholar] 47. Hu Y., Yang X., Qin J., Lu N., Cheng G., Wu N., Pan Y., Li J., Zhu L., Wang X., et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat. Commun. 2013;4:2151. doi: 10.1038/ncomms3151. [PubMed] [CrossRef] [Google Scholar] 48. Fitzpatrick D., Walsh F. Antibiotic resistance genes across a wide variety of metagenomes. FEMS Microbiol. Ecol. 2016;92:fiv168. doi: 10.1093/femsec/fiv168. [PubMed] [CrossRef] [Google Scholar] 49. Li Y., Cao W., Liang S., Yamasaki S., Chen X., Shi L., Ye L. Metagenomic characterization of bacterial community and antibiotic resistance genes in representative ready-to-eat food in southern China. Sci. Rep. 2020;10:15175. doi: 10.1038/s41598-020-72620-4. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 50. Auguet O.T., Niehus R., Gweon H.S., Berkley J.A., Waichungo J., Njim T., Edgeworth J.D., Batra R., Chau K., Swann J., et al. Population-level faecal metagenomic profiling as a tool to predict antimicrobial resistance in Enterobacterales isolates causing invasive infections: An exploratory study across Cambodia, Kenya, and the UK. EClinicalMedicine. 2021;36:100910. doi: 10.1016/j.eclinm.2021.100910. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 51. Naik O.A., Shashidhar R., Rath D., Bandekar J.R., Rath A. Characterization of multiple antibiotic resistance of culturable microorganisms and metagenomic analysis of total microbial diversity of marine fish sold in retail shops in Mumbai, India. Environ. Sci. Pollut. Res. Int. 2018;25:6228–6239. doi: 10.1007/s11356-017-0945-7. [PubMed] [CrossRef] [Google Scholar] 52. Noyes N.R., Yang X., Linke L.M., Magnuson R.J., Cook S.R., Zaheer R., Yang H., Woerner D.R. Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems. Sci. Rep. 2016;6:24645. doi: 10.1038/srep24645. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 53. Coughlan L.M., Cotter P.D., Hill C., Alvarez-Ordóñez A. Biotechnological applications of functional metagenomics in the food and pharmaceutical industries. Front. Microbiol. 2015;6:672. doi: 10.3389/fmicb.2015.00672. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 54. Leonard S.R., Mammel M.K., Lacher D.W., Elkins C.A. Application of metagenomic sequencing to food safety: Detection of Shiga Toxin-producing Escherichia coli on fresh bagged spinach. Appl. Environ. Microbiol. 2015;81:8183–8191. doi: 10.1128/AEM.02601-15. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 55. Walsh A.M., Crispie F., Daari K., O’Sullivan O., Martin J.C., Arthur C.T., Claesson M.J., Scott K.P., Cotter P. D Strain-Level Metagenomic Analysis of the Fermented Dairy Beverage Nunu Highlights Potential Food Safety Risks. Appl. Environ. Microbiol. 2017;83:e01144-17. doi: 10.1128/AEM.01144-17. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 56. Escobar-Zepeda A., Sanchez-Flores A., Quirasco Baruch M. Metagenomic analysis of a Mexican ripened cheese reveals a unique complex microbiota. Food Microbiol. 2016;57:116–127. doi: 10.1016/j.fm.2016.02.004. [PubMed] [CrossRef] [Google Scholar] 57. Huang A.D., Luo C., Pena-Gonzalez A., Weigand M.R., Tarr C.L., Konstantinidis K.T. Metagenomics of Two Severe Foodborne Outbreaks Provides Diagnostic Signatures and Signs of Coinfection Not Attainable by Traditional Methods. Appl. Environ. Microbiol. 2017;83:e02577-16. doi: 10.1128/AEM.02577-16. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 58. Ottesen A., Ramachandran P., Reed E., White J.R., Hasan N., Subramanian P., Ryan G., Jarvis K., Grim C., Daquiqan N., et al. Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak. BMC Microbiol. 2016;16:275. doi: 10.1186/s12866-016-0894-1. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 59. Yang X., Noyes N.R., Doster E., Martin J.N., Linke L.M., Magnuson R.J., Yang H., Geornaras I., Woerner D.R., Jones K.L., et al. Use of Metagenomic Shotgun Sequencing Technology to Detect Foodborne Pathogens within the Microbiome of the Beef Production Chain. Appl. Environ. Microbiol. 2016;82:2433–2443. doi: 10.1128/AEM.00078-16. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 60. Quigley L., O’Sullivan D.J., Daly D., O’Sullivan O., Burdikova Z., Vana R., Beresford T.P., Ross R.P., Fitzgerald G.F., McSweeney P.L.H., et al. Thermus and the Pink Discoloration Defect in Cheese. mSystems. 2016;1:e00023-16. doi: 10.1128/mSystems.00023-16. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 61. De Filippis F., Parente E., Ercolini D. Metagenomics insights into food fermentations. Microb. Biotechnol. 2017;10:91–102. doi: 10.1111/1751-7915.12421. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 62. Leech J., Cabrera-Rubio R., Walsh A.M., Macori G., Walsh C.J., Barton W., Finnegan L., Crispie F., O’Sullivan O., Claesson M.J., et al. Fermented-Food Metagenomics Reveals Substrate-Associated Differences in Taxonomy and Health-Associated and Antibiotic Resistance Determinants. mSystems. 2020;5:e00522-20. doi: 10.1128/mSystems.00522-20. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 63. Lorenz P., Eck J. Metagenomics and industrial applications. Nat. Rev. Microbiol. 2005;3:510–516. doi: 10.1038/nrmicro1161. [PubMed] [CrossRef] [Google Scholar] 64. Prayogo F.A., Budiharjo A., Kusumaningrum H.P., Wijanarka W., Suprihadi A., Nurhayati N. Metagenomic applications in exploration and development of novel enzymes from nature: A review. J. Genet. Eng. Biotechnol. 2020;18:39. doi: 10.1186/s43141-020-00043-9. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 65. Pabbathi N.P.P., Velidandi A., Tavarna T., Gupta S., Raj R.S., Gandam P.K., Baadhe R.R. Role of metagenomics in prospecting novel endoglucanases, accentuating functional metagenomics approach in second-generation biofuel production: A review. Biomass Convers. Biorefin. 2021;7:1–28. doi: 10.1007/s13399-020-01186-y. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 66. Bashir A.K., Wink L., Duller S., Schwendner P., Cockell C., Rettberg P., Mahnert A., Beblo-Vranesevic K., Bohmeier M., Rabbow E., et al. Taxonomic and functional analyses of intact microbial communities thriving in extreme, astrobiology-relevant, anoxic sites. Microbiome. 2021;9:50. doi: 10.1186/s40168-020-00989-5. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 67. Peimbert M., Alcaraz L.D., Bonilla-Rosso G., Olmedo-Alvarez G., García-Oliva F., Segovia L., Eguiarte L.E., Souza V. Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin I: Ancient lessons on how to cope with an environment under severe nutrient stress. Astrobiology. 2012;12:648–658. doi: 10.1089/ast.2011.0694. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 68. Be N.A., Avila-Herrera A., Allen J.E., Singh N., Checinska Sielaff A., Jaing C., Venkateswaran K. Whole metagenome profiles of particulates collected from the International Space Station. Microbiome. 2017;5:81. doi: 10.1186/s40168-017-0292-4. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 69. Bashir M., Ahmed M., Weinmaier T., Ciobanu D., Ivanova N., Pieber T.R., Vaishampayan P.A. Functional Metagenomics of Spacecraft Assembly Cleanrooms: Presence of Virulence Factors Associated with Human Pathogens. Front. Microbiol. 2016;7:1321. doi: 10.3389/fmicb.2016.01321. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 70. Singh N.K., Wood J.M., Karouia F., Venkateswaran K. Succession and persistence of microbial communities and antimicrobial resistance genes associated with International Space Station environmental surfaces. Microbiome. 2018;6:204. doi: 10.1186/s40168-018-0585-2. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 71. Mardanov A.V., Babykin M.M., Beletsky A.V., Grigoriev A.I., Zinchenko V.V., Kadnikov V.V., Kirpichnikov M.P., Mazur A.M., Nedoluzhko A.V., Novikova N.D., et al. Metagenomic Analysis of the Dynamic Changes in the Gut Microbiome of the Participants of the MARS-500 Experiment, Simulating Long Term Space Flight. Acta Nat. 2013;5:116–125. doi: 10.32607/20758251-2013-5-3-116-125. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 72. Avila-Herrera A., Thissen J., Urbaniak C., Be N.A., Smith D.J., Karouia F., Mehta S., Venkateswaran K., Jaing C. Crewmember microbiome may influence microbial composition of ISS habitable surfaces. PLoS ONE. 2020;15:e0231838. doi: 10.1371/journal.pone.0231838. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 73. Lee M.D., O’Rourke A., Lorenzi H., Bebout B.M., Dupont C.L., Everroad R.C. Reference-guided metagenomics reveals genome-level evidence of potential microbial transmission from the ISS environment to an astronaut’s microbiome. iScience. 2021;24:102114. doi: 10.1016/j.isci.2021.102114. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 74. Góes-Neto A., Kukharenko O., Orlovska I., Podolich O., Imchen M., Kumavath R., Kato R.B., Carvalho D.S., Tiwari S., Brenig B., et al. Shotgun metagenomic analysis of kombucha mutualistic community exposed to Mars-like environment outside the International Space Station. Environ. Microbiol. 2021;23:3727–3742. doi: 10.1111/1462-2920.15405. [PubMed] [CrossRef] [Google Scholar] 75. Orlovska I., Podolich O., Kukharenko O., Zaets I., Reva O., Khirunenko L., Zmejkoski D., Rogalsky S., Barh D., Tiwari S., et al. Bacterial Cellulose Retains Robustness but Its Synthesis Declines After Exposure to a Mars-like Environment Simulated Outside the International Space Station. Astrobiology. 2021;21:706–717. doi: 10.1089/ast.2020.2332. [PubMed] [CrossRef] [Google Scholar] 76. Singh N.K., Wood J.M., Mhatre S.S., Venkateswaran K. Metagenome to phenome approach enables isolation and genomics characterization of Kalamiella piersonii gen. nov.; sp. nov. from the International Space Station. Appl. Microbiol. Biotechnol. 2019;103:4483–4497. doi: 10.1007/s00253-019-09813-z. [PubMed] [CrossRef] [Google Scholar] 77. Yasir M., Angelakis E., Bibi F., Azhar E.I., Bachar D., Lagier J.-C., Gaborit B., Hassan A.M., Jiman-Fatani A.A., Alshali K.Z., et al. Comparison of the gut microbiota of people in France and Saudi Arabia. Nutr. Diabetes. 2015;5:e153. doi: 10.1038/nutd.2015.3. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 78. Angelakis E., Bachar D., Yasir M., Musso D., Djossou F., Melenotte C., Robert C., Davoust B., Gaborit B., Azhar E.I., et al. Comparison of the gut microbiota of obese individuals from different geographic origins. New Microbes New Infect. 2018;27:40–47. doi: 10.1016/j.nmni.2018.11.005. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 79. Bittar F., Bibi F., Ramasamy D., Lagier J.-C., Azhar E.I., Jiman-Fatani A.A., Al-Ghamdi A.K., Nguyen T.T., Yasir M., Fournier P.-E., et al. Non contiguous-finished genome sequence and description of Bacillus jeddahensis sp. nov. Stand. Genom. Sci. 2015;10:47. doi: 10.1186/s40793-015-0024-y. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 80. Khelaifia S., Lagier J.-C., Bibi F., Azhar E.I., Croce O., Padmanabhan R., Jiman-Fatani A.A., Yasir M., Robert C., Andrieu C., et al. Microbial Culturomics to Map Halophilic Bacterium in Human Gut: Genome Sequence and Description of Oceanobacillus jeddahense sp. nov. Omics. 2016;20:248–258. doi: 10.1089/omi.2016.0004. [PubMed] [CrossRef] [Google Scholar] 81. Kieu H.T., Garrigou N., Fadlane A., Brechard L., Armstrong N., Decloquement P., Yasir M., Azhar E.I., Al-Masaudi S.B., Lagier J.-C., et al. Clostridium culturomicium sp. nov. and Clostridium jeddahitimonense sp. nov.; novel members of the Clostridium genus isolated from the stool of an obese Saudi Arabian. Curr. Microbiol. 2021;74:3586–3595. doi: 10.1007/s00284-021-02616-4. [PubMed] [CrossRef] [Google Scholar] 82. Al-Obaida M.I., Al-Nakhli A.K.M., Arif I.A., Faden A., Al-Otaibi S., Al-Eid B., Ekhzaimy A., Khan H.A. Molecular identification and diversity analysis of dental bacteria in diabetic and non-diabetic females from Saudi Arabia. Saudi J. Biol. Sci. 2020;27:358–362. doi: 10.1016/j.sjbs.2019.10.005. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 83. Abdulhaq A., Halboub E., Homeida H.E., Kumar Basode V., Ghzwani A.H., Zain K.A., Baraniya D., Chen T., Al-Hebshi N.N. Tongue microbiome in children with autism spectrum disorder. J. Oral. Microbiol. 2021;13:1936434. doi: 10.1080/20002297.2021.1936434. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 84. Alzahrani F.M., Al-Amri A., Shaikh S.S., Alomar A.I., Acharya S., Aldossary M.A., Hassan F.M. Direct DNA Sequencing-Based Analysis of Microbiota Associated with Hematological Malignancies in the Eastern Province of Saudi Arabia. BioMed Res. Int. 2021;2021:4202019. doi: 10.1155/2021/4202019. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 85. Aljabr W., Alruwaili M., Penrice-Randal R., Alrezaihi A., Harrison A.J., Ryan Y., Bentley E., Jones B., Alhatlani B.Y., AlShahrani D., et al. Amplicon and Metagenomic Analysis of Middle East Respiratory Syndrome (MERS) Coronavirus and the Microbiome in Patients with Severe MERS. mSphere. 2021;21:e0021921. doi: 10.1128/mSphere.00219-21. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 86. Khan I., Yasir M., Farman M., Kumosani T., AlBasri S.F., Bajouh O.S., Azhar E.I. Evaluation of gut bacterial community composition and antimicrobial resistome in pregnant and non-pregnant women from Saudi population. Infect. Drug Resist. 2019;12:1749–1761. doi: 10.2147/IDR.S200213. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 87. Al Moaleem M.M., Porwal A., Al Ahmari N.M., Shariff M., Homeida H., Khalid A. Khat Chewing Induces a Floral Shift in Dental Material-Associated Microbiota: A Preliminary Study. Med. Sci. Monit. 2020;26:e918219. doi: 10.12659/MSM.918219. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 88. Badger-Emeka L.I., AlJaziri Z.Y., Almulhim C.F., Aldrees A.S., AlShakhs Z.H., AlAithan R.I., Alothman F.A. Vitamin D Supplementation in Laboratory-Bred Mice: An In Vivo Assay on Gut Microbiome and Body Weight. Microbiol. Insights. 2020;13:1178636120945294. doi: 10.1177/1178636120945294. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 89. Elbir H., Almathen F., Alhumam N.A. A glimpse of the bacteriome of Hyalomma dromedarii ticks infesting camels reveals human Helicobacter pylori pathogen. J. Infect. Dev. Ctries. 2019;13:1001–1012. doi: 10.3855/jidc.11604. [PubMed] [CrossRef] [Google Scholar] 90. Elbir H., Almathen F., Elnahas A. Low genetic diversity among Francisella-like endosymbionts within different genotypes of Hyalomma dromedarii ticks infesting camels in Saudi Arabia. Vet. World. 2020;13:1462–1472. doi: 10.14202/vetworld.2020.1462-1472. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 91. Alreshidi M.M., Veettil V.N., Noumi E., Campo R.D., Snoussi M. Description of microbial diversity associated with ticks Hyalomma dromedarii (Acari: Ixodidae) isolated from camels in Hail region (Saudi Arabia) using massive sequencing of 16S rDNA. Bioinformation. 2020;16:602–610. doi: 10.6026/97320630016602. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 92. Alzubaidy H., Essack M., Malas T.B., Bokhari A., Motwalli O., Kamanu F.K., Jamhor S.A., Mokhtar N.A., Antunes A., Simões M.F., et al. Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea. Gene. 2016;576:626–636. doi: 10.1016/j.gene.2015.10.032. [PubMed] [CrossRef] [Google Scholar] 93. Al-Quwaie D.A. Bacterial community dynamics with rhizosphere of Calotropis procera and Senna alexandrina desert plants in Saudi Arabia. Bioinformation. 2020;16:567–578. doi: 10.6026/97320630016567. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 94. Yasir M., Azhar E.I., Khan I., Bibi F., Baabdullah R., Al-Zahrani I.A., Al-Ghamdi A.K. Composition of soil microbiome along elevation gradients in southwestern highlands of Saudi Arabia. BMC Microbiol. 2015;15:65. doi: 10.1186/s12866-015-0398-4. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 95. Gat D., Mazar Y., Cytryn E., Rudich Y. Origin-Dependent Variations in the Atmospheric Microbiome Community in Eastern Mediterranean Dust Storms. Environ. Sci. Technol. 2017;51:6709–6718. doi: 10.1021/acs.est.7b00362. [PubMed] [CrossRef] [Google Scholar] 96. Yasir M., Qureshi A.K., Khan I., Bibi F., Rehan M., Khan S.B., Azhar E.I. Culturomics-Based Taxonomic Diversity of Bacterial Communities in the Hot Springs of Saudi Arabia. Omics. 2019;23:17–27. doi: 10.1089/omi.2018.0176. [PubMed] [CrossRef] [Google Scholar] 97. Yasir M., Qureshi A.K., Srinivasan S., Ullah R., Bibi F., Rehan M., Khan S.B., Azhar E.I. Domination of Filamentous Anoxygenic Phototrophic Bacteria and Prediction of Metabolic Pathways in Microbial Mats from the Hot Springs of Al Aridhah. Folia Biol. 2020;66:24–35. [PubMed] [Google Scholar] 98. Li D., Sharp J.O., Saikaly P.E., Ali S., Alidina M., Alarawi M.S., Keller S., Hoppe-Jones C., Drewes J.E. Dissolved organic carbon influences microbial community composition and diversity in managed aquifer recharge systems. Appl. Environ. Microbiol. 2012;78:6819–6828. doi: 10.1128/AEM.01223-12. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 99. Al-Jassim N., Ansari M.I., Harb M., Hong P.Y. Removal of bacterial contaminants and antibiotic resistance genes by conventional wastewater treatment processes in Saudi Arabia: Is the treated wastewater safe to reuse for agricultural irrigation? Water Res. 2015;73:277–290. doi: 10.1016/j.watres.2015.01.036. [PubMed] [CrossRef] [Google Scholar] 100. Bibi F., Alvi S.A., Al-Sofyani A., Naseer M.I., Yasir M., Azhar E.I. Pyrosequencing reveals sponge specific bacterial communities in marine sponges of Red Sea, Saudi Arabia. Saudi J. Biol. Sci. 2020;27:67–73. doi: 10.1016/j.sjbs.2019.05.002. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 101. Albokari M., Mashhour I., Alshehri M., Boothman C., Al-Enezi M. Characterization of microbial communities in heavy crude oil from Saudi Arabia. Ann. Microbiol. 2015;65:95–104. doi: 10.1007/s13213-014-0840-0. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 102. El-Sayed W.S., Ibrahim R.A. Diversity and phylogenetic analysis of endosymbiotic bacteria of the date palm root borer Oryctes agamemnon (Coleoptera: Scarabaeidae) BMC Microbiol. 2015;15:88. doi: 10.1186/s12866-015-0422-8. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 103. Moussa T.A., Al-Zahrani H.S., Almaghrabi O.A., Sabry N.M., Fuller M.P. Metagenomic analysis of fungal taxa inhabiting Mecca region, Saudi Arabia. Genom. Data. 2016;9:126–127. doi: 10.1016/j.gdata.2016.07.008. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 104. Soltani R., Lkbel C., Hamouda M.H.B. Descriptive study of damage caused by the rhinoceros beetle, Oryctes agamemnon, and its influence on date palm oases of Rjim Maatoug, Tunisia. J. Insect Sci. 2008;8:57. doi: 10.1673/031.008.5701. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 105. Sefrji F.O., Michoud G., Marasco R., Merlino G., Daffonchio D. Mangrovivirga cuniculi gen. nov.; sp. nov.; a moderately halophilic bacterium isolated from bioturbated Red Sea mangrove sediment, and proposal of the novel family Mangrovivirgaceae fam. nov. Int. J. Syst. Evol. Microbiol. 2021;71:004866. doi: 10.1099/ijsem.0.004866. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 106. Sefrji F.O., Marasco R., Michoud G., Seferji K.A., Merlino G., Daffonchio D. Kaustia mangrovi gen. nov.; sp. nov. isolated from Red Sea mangrove sediments belongs to the recently proposed Parvibaculaceae family within the order Rhizobiales. Int. J. Syst. Evol. Microbiol. 2021;71:004806. doi: 10.1099/ijsem.0.004806. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 107. Röttig A., Atasayar E., Meier-Kolthoff J.P., Spröer C., Schumann P., Schauer J., Steinbüchel A. Streptomyces jeddahensis sp. nov.; an oleaginous bacterium isolated from desert soil. Int. J. Syst. Evol. Microbiol. 2017;67:1676–1682. doi: 10.1099/ijsem.0.001839. [PubMed] [CrossRef] [Google Scholar] 108. Yang Z.W., Salam N., Hua Z.S., Liu B.B., Han M.X., Fang B.Z., Wang D., Xiao M., Hozzein W.N., Li W.J. Siccirubricoccus deserti gen. nov.; sp. nov.; a proteobacterium isolated from a desert sample. Int. J. Syst. Evol. Microbiol. 2017;67:4862–4867. doi: 10.1099/ijsem.0.002397. [PubMed] [CrossRef] [Google Scholar] 109. Wübbeler J.H., Oppermann-Sanio F.B., Ockenfels A., Röttig A., Osthaar-Ebker A., Verbarg S., Poehlein A., Madkour M.H., Al-Ansari A.M., Almakishah N.H., et al. Sphingomonas jeddahensis sp. nov.; isolated from Saudi Arabian desert soil. Int. J. Syst. Evol. Microbiol. 2017;67:4057–4063. doi: 10.1099/ijsem.0.002249. [PubMed] [CrossRef] [Google Scholar] 110. Yang Z.W., Salam N., Mohany M., Chinnathambi A., Alharbi S.A., Xiao M., Hozzein W.N., Li W.J. Microbacterium album sp. nov. and Microbacterium deserti sp. nov.; two halotolerant actinobacteria isolated from desert soil. Int. J. Syst. Evol. Microbiol. 2018;68:217–222. doi: 10.1099/ijsem.0.002485. [PubMed] [CrossRef] [Google Scholar] 111. Li L.Y., Yang Z.W., Asem M.D., Salam N., Xiao M., Alkhalifah D.H.M., Hozzein W.N., Nie G.X., Li W.J. Georgenia alba sp. nov.; a novel halotolerant actinobacterium isolated from a desert sand sample. Antonie Van Leeuwenhoek. 2019;112:203–209. doi: 10.1007/s10482-018-1145-2. [PubMed] [CrossRef] [Google Scholar] 112. Hozzein W.N., Yang Z.W., Alharbi S.A., Alsakkaf W.A.A., Asem M.D., Xiao M., Salam N., Li W.J. Georgenia deserti sp. nov.; a halotolerant actinobacterium isolated from a desert sample. Int. J. Syst. Evol. Microbiol. 2018;68:1135–1139. doi: 10.1099/ijsem.0.002640. [PubMed] [CrossRef] [Google Scholar] 113. Hussain F., Khan I.U., Habib N., Xian W.D., Hozzein W.N., Zhang Z.D., Zhi X.Y., Li W.J. Deinococcus saudiensis sp. nov.; isolated from desert. Int. J. Syst. Evol. Microbiol. 2016;66:5106–5111. doi: 10.1099/ijsem.0.001479. [PubMed] [CrossRef] [Google Scholar] 114. Almuhayawi M.S., Mohamed M.S.M., Abdel-Mawgoud M., Selim S., Al Jaouni S.K., AbdElgawad H. Bioactive Potential of Several Actinobacteria Isolated from Microbiologically Barely Explored Desert Habitat, Saudi Arabia. Biology. 2021;10:235. doi: 10.3390/biology10030235. [PMC free article] [PubMed] [CrossRef] [Google Scholar] 115. Wang J.-W., Kuo C.-H., Kuo F.-C., Wang Y.-K., Hsu W.-H., Yu F.-J., Hu H.-M., Hsu P.-I., Wang J.-Y., Wu D.C. Fecal microbiota transplantation: Review and update. J. Formos Med. Assoc. 2019;118:S23–S31. doi: 10.1016/j.jfma.2018.08.011. [PubMed] [CrossRef] [Google Scholar] 116. Ooijevaar R.E., Terveer E.M., Verspaget H.W., Kuijper E.J., Keller J.J. Clinical Application and Potential of Fecal Microbiota Transplantation. Annu. Rev. Med. 2019;70:335–351. doi: 10.1146/annurev-med-111717-122956. [PubMed] [CrossRef] [Google Scholar] 117. Dubilier N., McFall-Ngai M., Zhao L. Microbiology: Create a global microbiome effort. Nature. 2015;526:631–634. doi: 10.1038/526631a. [PubMed] [CrossRef] [Google Scholar]
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