Dissecting the HGT network of carbon metabolic genes in soil-borne microbiota.

Liangzhi Li, Yongjun Liu, Qinzhi Xiao, Zhipeng Xiao, Delong Meng, Zhaoyue Yang, Wenqiao Deng, Huaqun Yin, Zhenghua Liu
Author Information
  1. Liangzhi Li: School of Minerals Processing and Bioengineering, Central South University, Changsha, China.
  2. Yongjun Liu: Hunan Tobacco Science Institute, Changsha, China.
  3. Qinzhi Xiao: Yongzhou Tobacco Company of Hunan Province, Yongzhou, China.
  4. Zhipeng Xiao: Hengyang Tobacco Company of Hunan Province, Hengyang, China.
  5. Delong Meng: School of Minerals Processing and Bioengineering, Central South University, Changsha, China.
  6. Zhaoyue Yang: School of Minerals Processing and Bioengineering, Central South University, Changsha, China.
  7. Wenqiao Deng: Changsha Institute of Agricultural Science, Changsha, China.
  8. Huaqun Yin: School of Minerals Processing and Bioengineering, Central South University, Changsha, China.
  9. Zhenghua Liu: School of Minerals Processing and Bioengineering, Central South University, Changsha, China.

Abstract

The microbiota inhabiting soil plays a significant role in essential life-supporting element cycles. Here, we investigated the occurrence of horizontal gene transfer (HGT) and established the HGT network of carbon metabolic genes in 764 soil-borne microbiota genomes. Our study sheds light on the crucial role of HGT components in microbiological diversification that could have far-reaching implications in understanding how these microbial communities adapt to changing environments, ultimately impacting agricultural practices. In the overall HGT network of carbon metabolic genes in soil-borne microbiota, a total of 6,770 nodes and 3,812 edges are present. Among these nodes, phyla Proteobacteria, Actinobacteriota, Bacteroidota, and Firmicutes are predominant. Regarding specific classes, Actinobacteria, Gammaproteobacteria, Alphaproteobacteria, Bacteroidia, Actinomycetia, Betaproteobacteria, and Clostridia are dominant. The Kyoto Encyclopedia of Genes and Genomes (KEGG) functional assignments of glycosyltransferase (18.5%), glycolysis/gluconeogenesis (8.8%), carbohydrate-related transporter (7.9%), fatty acid biosynthesis (6.5%), benzoate degradation (3.1%) and butanoate metabolism (3.0%) are primarily identified. Glycosyltransferase involved in cell wall biosynthesis, glycosylation, and primary/secondary metabolism (with 363 HGT entries), ranks first overwhelmingly in the list of most frequently identified carbon metabolic HGT enzymes, followed by pimeloyl-ACP methyl ester carboxylesterase, alcohol dehydrogenase, and 3-oxoacyl-ACP reductase. Such HGT events mainly occur in the peripheral functions of the carbon metabolic pathway instead of the core section. The inter-microbe HGT genetic traits in soil-borne microbiota genetic sequences that we recognized, as well as their involvement in the metabolism and regulation processes of carbon organic, suggest a pervasive and substantial effect of HGT on the evolution of microbes.

Keywords

Associated Data

figshare | 10.6084/m9.figshare.22154828.v1

References

  1. Appl Environ Microbiol. 1996 Feb;62(2):515-21 [PMID: 8593052]
  2. Nucleic Acids Res. 2010 Jan;38(Database issue):D382-90 [PMID: 19864254]
  3. Appl Environ Microbiol. 1989 Jul;55(7):1730-4 [PMID: 2669634]
  4. Trends Ecol Evol. 2005 Jun;20(6):345-53 [PMID: 16701391]
  5. Appl Environ Microbiol. 1988 Dec;54(12):2916-23 [PMID: 16347789]
  6. Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20537-42 [PMID: 23184964]
  7. Genome Res. 2005 Jul;15(7):954-9 [PMID: 15965028]
  8. Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5602-7 [PMID: 17372208]
  9. Comput Struct Biotechnol J. 2020 Jun 10;18:1383-1390 [PMID: 32637037]
  10. Mol Biol Evol. 2012 Apr;29(4):1225-40 [PMID: 22130968]
  11. ISME J. 2015 Mar 17;9(4):934-45 [PMID: 25333461]
  12. BMC Evol Biol. 2015 Jun 05;15:102 [PMID: 26044078]
  13. New Phytol. 2022 Apr;234(1):64-76 [PMID: 35103312]
  14. Org Biomol Chem. 2003 Jan 7;1(1):39-41 [PMID: 12929388]
  15. Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):21748-53 [PMID: 20007373]
  16. Proc Natl Acad Sci U S A. 2007 May 8;104(19):7746-51 [PMID: 17470793]
  17. Nucleic Acids Res. 2013 Sep;41(16):7635-55 [PMID: 23814188]
  18. Front Microbiol. 2022 Jan 14;12:833172 [PMID: 35095829]
  19. Nature. 2005 Feb 24;433(7028):895-900 [PMID: 15729348]
  20. Appl Environ Microbiol. 1990 Feb;56(2):401-8 [PMID: 2106286]
  21. Sci Rep. 2016 Feb 16;6:21550 [PMID: 26878889]
  22. Nat Genet. 2005 Dec;37(12):1372-5 [PMID: 16311593]
  23. Annu Rev Genet. 2005;39:309-38 [PMID: 16285863]
  24. FEMS Microbiol Ecol. 2000 Jan 1;31(1):39-45 [PMID: 10620717]
  25. Nat Chem Biol. 2010 Sep;6(9):682-8 [PMID: 20693992]
  26. Sci Adv. 2021 Oct 22;7(43):eabj5056 [PMID: 34678056]
  27. Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14332-7 [PMID: 16176988]
  28. Nat Rev Genet. 2007 Jun;8(6):450-61 [PMID: 17510665]
  29. Infect Immun. 2017 Mar 23;85(4): [PMID: 28167670]
  30. mSphere. 2016 Sep 14;1(5): [PMID: 27642638]
  31. Mol Biol Evol. 2006 Feb;23(2):254-67 [PMID: 16221896]
  32. Appl Environ Microbiol. 1989 Apr;55(4):1029-32 [PMID: 2729977]
  33. Genome Biol Evol. 2013;5(12):2305-17 [PMID: 24259310]
  34. Philos Trans R Soc Lond B Biol Sci. 2022 Aug 15;377(1857):20210395 [PMID: 35757882]
  35. Eur J Biochem. 1998 Jun 1;254(2):356-62 [PMID: 9660191]
  36. Nat Rev Microbiol. 2017 Oct;15(10):579-590 [PMID: 28824177]
  37. New Phytol. 2023 Feb;237(4):1333-1346 [PMID: 36305241]
  38. mSystems. 2021 Aug 31;6(4):e0060221 [PMID: 34254817]
  39. ISME J. 2020 Feb;14(2):463-475 [PMID: 31659233]
  40. Mol Gen Genet. 1978 Nov 9;166(3):287-90 [PMID: 105243]
  41. Nat Commun. 2017 Jun 07;8:15784 [PMID: 28589945]
  42. J Eukaryot Microbiol. 2012 Mar-Apr;59(2):105-10 [PMID: 22299709]
  43. FEMS Microbiol Ecol. 2007 Jan;59(1):167-76 [PMID: 17069619]
  44. Mol Plant Pathol. 2019 Dec;20(12):1696-1709 [PMID: 31560825]
  45. Appl Environ Microbiol. 1997 May;63(5):1980-6 [PMID: 16535608]
  46. Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15076-81 [PMID: 18806222]
  47. Mol Biol Evol. 2011 Apr;28(4):1481-9 [PMID: 21149642]
  48. PLoS One. 2012;7(5):e35846 [PMID: 22567114]
  49. Soil Biol Biochem. 2019 Sep;136:107521 [PMID: 31700196]
  50. J Biol Chem. 2010 Nov 26;285(48):37121-7 [PMID: 20870714]
  51. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3801-6 [PMID: 10097118]
  52. Nat Rev Genet. 2005 May;6(5):361-75 [PMID: 15861208]
  53. Genome Biol Evol. 2019 Feb 1;11(2):362-379 [PMID: 30629162]
  54. Microbes Environ. 2016 Dec 23;31(4):369-377 [PMID: 27645100]
  55. Int J Mol Sci. 2022 May 13;23(10): [PMID: 35628255]
  56. Front Microbiol. 2018 Jun 18;9:1285 [PMID: 29967598]
  57. Trends Microbiol. 2007 Feb;15(2):54-62 [PMID: 17184993]
  58. Antonie Van Leeuwenhoek. 2019 Oct;112(10):1553-1558 [PMID: 31129890]
  59. J Theor Biol. 2018 Oct 7;454:53-59 [PMID: 29859211]
  60. J Gen Microbiol. 1989 Feb;135(Pt 2):409-24 [PMID: 2515247]
  61. Acta Biochim Pol. 2012;59(3):345-51 [PMID: 22826823]
  62. Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2043-9 [PMID: 17261804]
  63. PLoS One. 2014 Jul 11;9(7):e100890 [PMID: 25013926]
  64. mBio. 2010 Oct 05;1(4): [PMID: 20941329]
  65. Cold Spring Harb Perspect Biol. 2016 Apr 01;8(4):a018036 [PMID: 26801681]
  66. Appl Environ Microbiol. 2006 Oct;72(10):6687-92 [PMID: 17021220]
  67. J Mol Evol. 2018 Apr;86(3-4):190-203 [PMID: 29556740]
  68. Nat Chem Biol. 2018 Jun;14(6):556-564 [PMID: 29713061]
  69. Nat Commun. 2017 Oct 20;8(1):1063 [PMID: 29051484]
  70. Environ Microbiol. 2020 Mar;22(3):934-951 [PMID: 31361937]
  71. mBio. 2016 Jul 12;7(4): [PMID: 27406565]
  72. Bioessays. 2013 Oct;35(10):868-75 [PMID: 24037739]
  73. Appl Environ Microbiol. 1997 Feb;63(2):679-86 [PMID: 16535521]
  74. Appl Microbiol Biotechnol. 2004 Apr;64(2):154-74 [PMID: 14689248]
  75. Appl Environ Microbiol. 2019 Jan 9;85(2): [PMID: 30389769]
  76. Microb Ecol. 2015 Jul;70(1):141-53 [PMID: 25542203]
  77. Philos Trans R Soc Lond B Biol Sci. 2009 Aug 12;364(1527):2275-89 [PMID: 19571247]
  78. Nature. 2001 May 3;411(6833):41-2 [PMID: 11333967]
  79. Mol Biol Evol. 2002 Dec;19(12):2226-38 [PMID: 12446813]
  80. Biotechnol Adv. 2019 Nov 1;37(6):107372 [PMID: 30880142]
  81. Genome Res. 2011 Apr;21(4):599-609 [PMID: 21270172]
  82. ISME J. 2019 Aug;13(8):2031-2043 [PMID: 30952996]
  83. PLoS One. 2016 Feb 11;11(2):e0147492 [PMID: 26866478]
  84. Front Microbiol. 2022 Aug 04;13:936267 [PMID: 35992716]
  85. Front Plant Sci. 2022 Nov 02;13:1025122 [PMID: 36407614]
  86. FEMS Microbiol Ecol. 2002 Nov 1;42(2):199-208 [PMID: 19709279]
  87. Trends Microbiol. 2002 Jan;10(1):1-4 [PMID: 11755071]
  88. ISME J. 2020 Jul;14(7):1834-1846 [PMID: 32327732]
  89. Nat Rev Microbiol. 2005 Sep;3(9):711-21 [PMID: 16138099]
  90. J Bacteriol. 1999 Mar;181(5):1585-602 [PMID: 10049392]
  91. Mol Biol Evol. 2017 Apr 1;35(4):899-913 [PMID: 29346651]
  92. Chem Soc Rev. 2014;43(20):6954-81 [PMID: 25017039]
  93. J Bacteriol. 2004 Jun;186(12):3862-72 [PMID: 15175300]
  94. Nature. 2007 Aug 23;448(7156):925-8 [PMID: 17713534]
  95. Mol Biol Evol. 2011 Feb;28(2):1057-74 [PMID: 21059789]
  96. mSystems. 2020 Nov 17;5(6): [PMID: 33203689]
  97. Nucleic Acids Res. 2019 Jan 8;47(D1):D309-D314 [PMID: 30418610]
  98. Curr Biol. 2022 Nov 21;32(22):4941-4948.e3 [PMID: 36223775]
  99. Genome Res. 2002 Apr;12(4):532-42 [PMID: 11932238]

Word Cloud

Created with Highcharts 10.0.0HGTcarbonmicrobiotametabolicnetworksoil-bornegenegenes3metabolismsoilrolehorizontaltransfer6nodes5%biosynthesisidentifiedgeneticinhabitingplayssignificantessentiallife-supportingelementcyclesinvestigatedoccurrenceestablished764genomesstudyshedslightcrucialcomponentsmicrobiologicaldiversificationfar-reachingimplicationsunderstandingmicrobialcommunitiesadaptchangingenvironmentsultimatelyimpactingagriculturalpracticesoveralltotal770812edgespresentAmongphylaProteobacteriaActinobacteriotaBacteroidotaFirmicutespredominantRegardingspecificclassesActinobacteriaGammaproteobacteriaAlphaproteobacteriaBacteroidiaActinomycetiaBetaproteobacteriaClostridiadominantKyotoEncyclopediaGenesGenomesKEGGfunctionalassignmentsglycosyltransferase18glycolysis/gluconeogenesis88%carbohydrate-relatedtransporter79%fattyacidbenzoatedegradation1%butanoate0%primarilyGlycosyltransferaseinvolvedcellwallglycosylationprimary/secondary363entriesranksfirstoverwhelminglylistfrequentlyenzymesfollowedpimeloyl-ACPmethylestercarboxylesterasealcoholdehydrogenase3-oxoacyl-ACPreductaseeventsmainlyoccurperipheralfunctionspathwayinsteadcoresectioninter-microbetraitssequencesrecognizedwellinvolvementregulationprocessesorganicsuggestpervasivesubstantialeffectevolutionmicrobesDissecting

Similar Articles

Cited By