Applied Microbiology and Biotechnology

, Volume 102, Issue 15, pp 6309–6318 | Cite as

Role of anaerobic bacteria in biological soil disinfestation for elimination of soil-borne plant pathogens in agriculture

  • Atsuko UekiEmail author
  • Nobuo Kaku
  • Katsuji Ueki


Biological soil disinfestation (BSD) or reductive soil disinfestation (RSD) is an environmental biotechnology to eliminate soil-borne plant pathogens based on functions of indigenous microbes. BSD treatments using different types of organic materials have been reported to effectively control a wide range of plant pathogens. Various studies have shown that development of reducing or anoxic conditions in soil is the most important aspect for effective BSD treatments. Substances such as organic acids, FeS, or phenolic compounds generated in the treated soil have been suggested to contribute to inactivation of pathogens. Additionally, anaerobic bacteria grown in the BSD-treated soil may produce and release enzymes with anti-pathogenic activities in soil. Clone library analyses as well as a next-generation sequence analysis based on 16S rRNA genes have revealed prosperity of obligate anaerobic bacteria from the class Clostridia in differently treated BSD soils. Two anaerobic bacterial strains isolated from BSD-treated soil samples and identified as Clostridium beijerinckii were found to decompose major cell wall polysaccharides of ascomycetous fungi, chitosan and β-1,3-glucan. C. beijerinckii is a species most frequently detected in the clone library analyses for various BSD-treated soils as a closely related species. The two anaerobic isolates severely degraded mycelial cells of the Fusarium pathogen of spinach wilt disease during anaerobic co-incubation of each isolate and the Fusarium pathogen. These reports suggest that antifungal enzymes produced by predominant anaerobic bacteria grown in the BSD-treated soil play important roles to control soil-borne fungal pathogens. Further studies using different bacterial isolates from BSD-treated soils are expected to know their anti-pathogenic abilities.


Anaerobic bacteria Anaerobic soil disinfestation (ASD) β-1,3-Glucan Biocontrol of soil-borne pathogen Chitosan Clostridium beijerinckii Fusarium oxysporum Reductive soil disinfestation (RSD) 



We would like to thank T. Takehara and G. Ishioka (NARO Western Region Agricultural Research Center) for their fruitful discussions. We greatly appreciate S. Mowlick who worked with us in our project.

Funding information

This study was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Science and technology research promotion program for agriculture, forestry, fisheries and food industry, No. 27016C).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interest.

Ethical approval

This article does not contain any studies concerned with experimentation on human or animals.


  1. Akasaka H, Izawa T, Ueki K, Ueki A (2003) Phylogeny of numerically abundant culturable anaerobic bacteria associated with degradation of rice plant residue in Japanese paddy field soil. FEMS Microbiol Ecol 43:149–161CrossRefPubMedGoogle Scholar
  2. Aktuganov GE, Galimzyanova NF, Melent’ev AI, Kuz’mina LY (2007) Extracellular hydrolases of strain Bacillus sp. 739 and their involvement in the lysis of micromycete cell walls. Microbiology 76:471–479CrossRefPubMedGoogle Scholar
  3. Bailey KL, Lazarovits G (2003) Suppressing soil borne diseases with residue management and organic amendments. Soil Till Res 72:169–180CrossRefGoogle Scholar
  4. Barko PC, McMichael MA, Swanson KS, Williams DA (2018) The gastrointestinal microbiome: a review. J Vet Intern Med 32:9–25CrossRefPubMedGoogle Scholar
  5. Blok WJ, Lamers JG, Termorshuizen AJ, Bollen GJ (2000) Control of soil-borne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology 90:253–259CrossRefPubMedGoogle Scholar
  6. Butler DM, Kokalis-Burelle N, Muramoto J, Shennan C, McCollum TG, Rosskopf EN (2012) Impact of anaerobic soil disinfestation combined with soil solarization on plant-parasitic nematodes and introduced inoculum of soilborne plant pathogens in raised-bed vegetable production. Crop Prot 39:33–40CrossRefGoogle Scholar
  7. Butler DM, Kokalis-Burelle N, Albano JP, McCollum TG, Muramoto J, Shennan C, Rosskopf EN (2014) Anaerobic soil disinfestation (ASD) combined with soil solarization as a methyl bromide alternative: vegetable crop performance and soil nutrient dynamics. Plant Soil 378:365–381CrossRefGoogle Scholar
  8. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JAE (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812–826CrossRefPubMedGoogle Scholar
  9. Cota IE, Troncoso-Rojas R, Sotelo-Mundo R, Sánches-Estrada A, Tiznado-Hernández ME (2007) Chitinase and β-1,3-glucanase enzymatic activities in response to infection by Alternaria alternata evaluated in two stages of development in different tomato fruit varieties. Sci Hortic 112:42–50CrossRefGoogle Scholar
  10. Di Gioia F, Ozores-Hampton M, Zhao X, Thomas J, Wilson P, Li Z, Hong J, Albano J, Swisher M, Rosskopf E (2017) Anaerobic soil disinfestation impact on soil nutrients dynamics and nitrous oxide emissions in fresh-market tomato. Agric Ecosyst Environ 240:194–205CrossRefGoogle Scholar
  11. Dvortsov IA, Lunina NA, Chekanovskaya LA, Schwarz WH, Zverlov VV, Velikodvorskaya GA (2009) Carbohydrate-binding properties of a separately folding protein module from β-1,3-glucanase Lic16A of Clostridium thermocellum. Microbiology 155:2442–2449CrossRefPubMedGoogle Scholar
  12. Egea C, Dickinson MJ, Candela M, Candela ME (1999) β-1,3-Glucanase isoenzymes and genes in resistant and susceptible pepper (Capsicum annuum) cultivars infected with Phytophthora capsici. Physiol Plant 107:312–318CrossRefGoogle Scholar
  13. Evvyernie D, Yamazaki S, Morimoto K, Karita S, Kimura T, Sakka K, Ohmiya K (2000) Identification and characterization of Clostridium paraputrificum M-21, a chitinolytic, mesophilic and hydrogen-producing bacterium. J Biosci Bioeng 89:596–601CrossRefPubMedGoogle Scholar
  14. Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390CrossRefPubMedGoogle Scholar
  15. Gavala HN, Angelidaki I, Ahring BK (2003) Kinetics and modeling of anaerobic digestion process. In: Biomethanation I (ed) Ahring BK. Springer-Verlag, Berlin, pp 57–93Google Scholar
  16. Goud JKC, Termorshuizen AJ, Blok WJ, van Bruggen AHC (2004) Long-term effect of biological soil disinfestation on Verticillium wilt. Plant Dis 88:688–694CrossRefGoogle Scholar
  17. Großkopf R, Stubner S, Liesack W (1998) Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl Environ Microbiol 64:4983–4989PubMedCentralGoogle Scholar
  18. Henckel T, Friedrich M, Conrad R (1999) Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Appl Environ Microbiol 65:1980–1990PubMedPubMedCentralGoogle Scholar
  19. Hengstmann D, Chin K-J, Janssen PH, Liesack W (1999) Comparative phylogenetic assignment of environmental sequences of genes encoding 16S rRNA and numerically abundant culturable bacteria from an anoxic rice paddy soil. Appl Environ Microbiol 65:5050–5058PubMedPubMedCentralGoogle Scholar
  20. Hillman ETLH, Yao T, Nakatsu CH (2017) Microbial ecology along the gastrointestinal tract. Microbes Environ 32:300–313CrossRefPubMedPubMedCentralGoogle Scholar
  21. Holdeman LV, Cato EP, Moore WEC (1977) Anaerobe laboratory manual, 4th edn. Virginia Polytechnic Institute and State University, BlacksburgGoogle Scholar
  22. Huang X, Liu L, Wen T, Zhang J, Wang F, Cai Z (2016) Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biotechnol 100:5581–5593CrossRefPubMedGoogle Scholar
  23. Huang X, Cui H, Yang L, Lan T, Zhang J, Cai Z (2017) The microbial changes during the biological control of cucumber damping-off disease using biocontrol agents and reductive soil disinfestation. BioControl 62:97–109CrossRefGoogle Scholar
  24. Ibekwe AM, Papiernik SK, Gan J, Yates SR, Yang CH, Crowley DE (2001) Impact of fumigants on soil microbial communities. Appl Environ Microbiol 67:3245–3257CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ibekwe AM, Papiernik SK, Yang CH (2004) Enrichment and molecular characterization of chloropicrin and metam-sodium-degrading microbial communities. Appl Microbiol Biotechnol 66:325–332CrossRefPubMedGoogle Scholar
  26. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728CrossRefPubMedPubMedCentralGoogle Scholar
  27. Katan J (1981) Solar heating (solarization) of soil for control of soil-borne pests. Annu Rev Phytopathol 19:211–236CrossRefGoogle Scholar
  28. Katan J (2000) Physical and cultural methods for the management of soil-borne pathogens. Crop Prot 19:25–31Google Scholar
  29. Katan J (2017) Disease caused by soilborne pathogens: biology, management and challenges. J Plant Pathol 99:305–315Google Scholar
  30. Kirkegaard JA, Wong PTW, Desmarchelier JM (1996) In-vitro suppression of fungal root pathogens of cereals by Brassica tissues. Plant Pathol 45:593–603CrossRefGoogle Scholar
  31. Kubo C, Ushio S, Katase M, Takeuchi T (2005) Analysis of factors involved in sterilization effect by soil reduction. Jpn J Phytopathol 71:281–282CrossRefGoogle Scholar
  32. Kurakake M, Yamanouchi Y, Kinohara K, Moriyama S (2013) Enzymatic properties of β-1,3-glucanase from Streptomyces sp Mo. J Food Sci 78:C502–C506CrossRefPubMedGoogle Scholar
  33. Larkin RP, Griffin TS (2007) Control of soil-borne potato diseases using Brassica green manures. Crop Prot 26:1067–1077CrossRefGoogle Scholar
  34. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lawson PA, Rainey FA (2016) Proposal to restrict the genus Clostridium (Prazmowski) to Clostridium butyricum and related species. Int J Syst Evol Microbiol 66:1009–1016CrossRefPubMedGoogle Scholar
  36. Liu L, Kong J, Cui H, Zhang J, Wang F, Cai Z, Huang X (2016) Relationships of decomposability and C/N ratio in different types of organic matter with suppression of Fusarium oxysporum and microbial communities during reductive soil disinfestation. Biol Control 101:103–113CrossRefGoogle Scholar
  37. Ludwig W, Schleifer K-H, Whitman WB (2009) Class III. Erysipelotricha class. nov. In: Whitman WB, Parte AC (eds) Bergey’s manual of systematic bacteriology, vol 3. Springer, New York, pp 1296–1317Google Scholar
  38. Macfarlane J, Macfarlane GT (1995) Proteolysis and amino acid fermentation. In: Gibson GR, Macfarlane GT (eds) Human colonic bacteria. CRC Press, New York, pp 75–100Google Scholar
  39. Mao L, Jiang H, Zhang L, Zhang Y, Sial MU, Yu H, Cao A (2017) Replacing methyl bromide with a combination of 1,3-dichloropropene and metam sodium for cucumber production in China. PLoS One 12:e0188137CrossRefPubMedPubMedCentralGoogle Scholar
  40. Marchandin H, Teyssier C, Campos J, Jean-Pierre H, Roger F, Gay B, Carlier J-P, Jumas-Bilak E (2010) Negativicoccus succinicivorans gen. nov., sp. nov., isolated from human clinical samples, emended description of the family Veillonellaceae and description of Negativicutes classis nov., Selenomonadales ord. nov. and Acidaminococcaceae fam. nov. in the bacterial phylum Firmicutes. Int J Syst Evol Microbiol 60:1271–1279CrossRefPubMedGoogle Scholar
  41. Mattner SW, Porter IJ, Gounder RK, Shanks AL, Wren DJ, Allen D (2008) Factors that impact on the ability of biofumigants to suppress fungal pathogens and weeds of strawberry. Crop Prot 27:1165–1173CrossRefGoogle Scholar
  42. McCarty DG, Inwood SEE, Ownley BH, Sams CE, Wszelaki AL, Butler DM (2014) Field evaluation of carbon sources for anaerobic soil disinfestation in tomato and bell pepper production in Tennessee. Hortscience 49:272–280Google Scholar
  43. Meng T, Yang Y, Cai Z, Ma Y (2018) The control of Fusarium oxysporum in soil treated with organic material under anaerobic condition is affected by liming and sulfate content. Biol Fertile Soils 54:295–307CrossRefGoogle Scholar
  44. Messiha NAS, van Diepeningen AD, Wenneker M, van Beuningen AR, Janse JD, Coenen TGC, Termorshuizen AJ, van Bruggen AHC, Blok WJ (2007) Biological soil disinfestation (BSD), a new control method for potato brown rot, caused by Ralstonia solanacearum race 3 biovar 2. Eur J Plant Pathol 117:403–415CrossRefGoogle Scholar
  45. Mojtahedi H, Santo GS, Hang AN, Wilson JH (1991) Suppression of root-knot nematode populations with selected rapeseed cultivars as green manure. J Nematol 23:170–174PubMedPubMedCentralGoogle Scholar
  46. Momma N, Yamamoto K, Simandi P, Shishido M (2006) Role of organic acids in the mechanisms of biological soil disinfestation (BSD). J Gen Plant Pathol 72:247–252CrossRefGoogle Scholar
  47. Momma N, Momma M, Kobara Y (2010) Biological soil disinfestation using ethanol: effect on Fusarium oxysporum f. sp. lycopersici and soil microorganisms. J Gen Plant Pathol 76:336–344CrossRefGoogle Scholar
  48. Momma N, Kobara Y, Momma M (2011) Fe2+ and Mn2+, potential agents to induce suppression of Fusarium oxysporum for biological soil disinfestation. J Gen Plant Pathol 77:331–335CrossRefGoogle Scholar
  49. Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A (2013) Development of biological soil disinfestations in Japan. Appl Microbiol Biotechnol 97:3801–3809CrossRefPubMedGoogle Scholar
  50. Mowlick S, Hirota K, Takehara T, Kaku N, Ueki K, Ueki A (2012) Development of anaerobic bacterial community consisted of diverse clostridial species during biological soil disinfestations amended with plant biomass. Soil Sci Plant Nutr 58:273–287CrossRefGoogle Scholar
  51. Mowlick S, Inoue T, Takehara T, Kaku N, Ueki K, Ueki A (2013a) Changes and recovery of soil bacterial communities influenced by biological soil disinfestation as compared with chloropicrin-treatment. AMB Express 3:46CrossRefPubMedPubMedCentralGoogle Scholar
  52. Mowlick S, Takehara T, Kaku N, Ueki K, Ueki A (2013b) Proliferation of diversified clostridial species during biological soil disinfestation incorporated with plant biomass under various conditions. Appl Microbiol Biotechnol 97:8365–8379CrossRefPubMedGoogle Scholar
  53. Mowlick S, Yasukawa H, Inoue T, Takehara T, Kaku N, Ueki K, Ueki A (2013c) Suppression of spinach wilt disease by biological soil disinfestation incorporated with Brassica juncea plants in association with changes in soil bacterial communities. Crop Prot 54:185–193CrossRefGoogle Scholar
  54. Mowlick S, Inoue T, Takehara T, Tonouchi A, Kaku N, Ueki K, Ueki A (2014) Usefulness of Japanese-radish residue in biological soil disinfestation to suppress spinach wilt disease accompanying with proliferation of soil bacteria in the Firmicutes. Crop Prot 61:64–73CrossRefGoogle Scholar
  55. Muramoto J, Shennan C, Baird G, Zavatta M, Koike ST, Bolda MP, Daugovish O, Dara SK, Klonsky K, Mazzola M (2014) Optimizing anaerobic soil disinfestation for California strawberries. Acta Hortic 1044:215–220CrossRefGoogle Scholar
  56. Nishiyama T, Ueki A, Kaku N, Watanabe K, Ueki K (2009) Bacteroides graminisolvens sp. nov., a novel, xylanolytic anaerobic rods isolated from a methanogenic reactor of cattle waste. Int J Syst Evol Microbiol 59:1901–1907CrossRefPubMedGoogle Scholar
  57. Peters V, Conrad R (1996) Sequential reduction processes and initiation of CH4 production upon flooding of oxic upland soils. Soil Biol Biochem 28:371–382CrossRefGoogle Scholar
  58. Prasanna R, Nain L, Tripathi R, Gupta V, Chaudhary V, Middha S, Joshi M, Ancha R, Kaushik BD (2008) Evaluation of fungicidal activity of extracellular filtrates of cyanobacteria—possible role of hydrolytic enzymes. J Basic Microbiol 48:186–194CrossRefPubMedGoogle Scholar
  59. Prather MJ, McElroy MB, Wofsy SC (1984) Reductions in ozone at high concentrations of stratospheric halogens. Nature 312:227–231CrossRefPubMedGoogle Scholar
  60. Rainey FA, Hollen BJ, Small A (2009) Genus I. Clostridium Prazmowski 1880, 23AL. In: Whitman WB, Parte AC (eds) Bergey’s manual of systematic bacteriology, vol 3. Springer, New York, pp 736–828Google Scholar
  61. Ristaino JB, Thomas W (1997) Agriculture, methyl bromide, and the ozone hole: can we fill the gaps. Plant Dis 81:954–975CrossRefGoogle Scholar
  62. Ruiz-Herrera J, Ortiz-Castellanos L (2010) Analysis of the phylogenetic relationships and evolution of the cell walls from yeasts and fungi. FEMS Yeast Res 10:225–243CrossRefPubMedGoogle Scholar
  63. Sandaa RA, Torsvik V, Enger O, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251CrossRefPubMedGoogle Scholar
  64. Sarwar M, Kirkegaard JA (1998) Biofumigation potential of brassicas. Plant Soil 201:91–101CrossRefGoogle Scholar
  65. Satoh A, Watanabe M, Ueki A, Ueki K (2002) Physiological properties and phylogenetic affiliations of anaerobic bacteria isolated from roots of rice plants cultivated on a paddy field. Anaerobe 8:233–246CrossRefGoogle Scholar
  66. Schink B (1999a) Habitat of prokaryotes. In: Lengeler JW, Drews G, Schlegel HG (eds) Biology of the prokaryotes. Blackwell Science, Stuttgart, pp 763–803Google Scholar
  67. Schink B (1999b) Global biogeochemical cycles. In: Lengeler JW, Drews G, Schlegel HG (eds) Biology of the prokaryotes. Blackwell Science, Stuttgart, pp 804–811Google Scholar
  68. Schoffelmeer EAM, Klis FM, Sietsma JH, Cornelissen BJC (1999) The cell wall of Fusarium oxysporum. Fungal Genet Biol 27:275–282CrossRefPubMedGoogle Scholar
  69. Sekiguchi Y, Kamagata Y (2004) Microbial community structure and functions in fermentation technology for wastewater treatment. In: Nakano MM, Zuber P (eds) Strict and facultative anaerobes: medical and environmental aspects. Horizon Bioscience, Norfolk, pp 361–383Google Scholar
  70. Serrano-Pérez P, Rosskopf E, De Santiago A, Rodríguez-Molina MC (2017) Anaerobic soil disinfestation reduces survival and infectivity of Phytophthora nicotianae chlamydospores in pepper. Sci Hort 215:38–48CrossRefGoogle Scholar
  71. Stackebrandt E (2004) The phylogeny and classification of anaerobic bacteria. In: Nakano MM, Zuber P (eds) Strict and facultative anaerobes: medical and environmental aspects. Horizon Bioscience, Norfolk, pp 1–25Google Scholar
  72. Stover RH (1979) Flooding of soil for disease control. In: Mulder D (ed) Soil disinfestation. Elsevier Scientific Company, Amsterdam, pp 19–28CrossRefGoogle Scholar
  73. Strauss SL, Kluepfel DA (2015) Anaerobic soil disinfestation: a chemical-independent approach to pre-plant control of plant pathogens. J Integ Agric 14:2309–2318CrossRefGoogle Scholar
  74. Subbarao KV (2002) Methyl bromide alternatives-meeting the deadline. Phytopathology 92:1334–1343CrossRefPubMedGoogle Scholar
  75. Sugawara Y, Ueki A, Abe K, Kaku N, Watanabe K, Ueki K (2011) Propioniciclava tarda gen. nov., sp. nov., isolated from a methanogenic reactor treating waste from cattle farms. Int J Syst Evol Microbiol 61:2298–2303CrossRefPubMedGoogle Scholar
  76. Takehara T, Kuniyasu K, Mori M, Hagiwara H (2003) Use of a nitrate-nonutilizing mutant and selective media to examine population dynamics of Fusarium oxysporum f. sp. spinaciae in soil. Phytopathology 93:1173–1181CrossRefPubMedGoogle Scholar
  77. Tanaka S, Kobayashi T, Iwasaki K, Yamane S, Maeda K, Sakurai K (2003) Properties and metabolic diversity of microbial communities in soils treated with steam sterilization compared with methyl bromide and chloropicrin fumigations. Soil Sci Plant Nutr 49:603–610CrossRefGoogle Scholar
  78. Trosvik P, de Muinck EJ (2015) Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa. Microbiome 3:44CrossRefPubMedPubMedCentralGoogle Scholar
  79. Ueki A, Akasaka H, Suzuki D, Ueki K (2006) Paludibacter propionicigenes gen. nov., sp. nov., a novel strictly anaerobic, Gram-negative, propionate-producing bacterium isolated from plant residue in irrigated rice-field soil in Japan. Int J Syst Evol Microbiol 56:39–44CrossRefPubMedGoogle Scholar
  80. Ueki A, Akasaka H, Satoh A, Suzuki D, Ueki K (2007) Prevotella paludivivens sp. nov., a novel strictly-anaerobic, Gram-negative, hemicellulose-decomposing bacterium isolated from plant residue and rice roots in irrigated rice-field soil. Int J Syst Evol Microbiol 57:1803–1809Google Scholar
  81. Ueki A, Abe K, Kaku N, Watanabe K, Ueki K (2008) Bacteroides propionicifaciens sp. nov., isolated from rice-straw residue in a methanogenic reactor treating waste from cattle farms. Int J Syst Evol Microbiol 58:346–352CrossRefPubMedGoogle Scholar
  82. Ueki A, Takehara T, Ishioka G, Kaku K, Ueki K (2017) Degradation of the fungal cell wall by clostridial strains isolated from soil subjected to biological soil disinfestation and biocontrol of Fusarium wilt disease of spinach. Appl Microbiol Biotechnol 101:8267–8277CrossRefPubMedGoogle Scholar
  83. Větrovský T, Baldrian P (2013) The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One 8:e57923CrossRefPubMedPubMedCentralGoogle Scholar
  84. Zehnder AJB (ed) (1988) Biology of anaerobic microorganisms. Wiley Interscience, New YorkGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of AgricultureYamagata UniversityTsuruokaJapan

Personalised recommendations