Genome sequences of lower Great Lakes Microcystis sp. reveal strain-specific genes that are present and expressed in western Lake Erie blooms.

Kevin Anthony Meyer, Timothy W Davis, Susan B Watson, Vincent J Denef, Michelle A Berry, Gregory J Dick
Author Information
  1. Kevin Anthony Meyer: Cooperative Institute for Great Lakes Research (CIGLR), University of Michigan, Ann Arbor, MI, United States of America. ORCID
  2. Timothy W Davis: NOAA Great Lakes Environmental Research Laboratory, Ann Arbor, MI, United States of America.
  3. Susan B Watson: Environment and Climate Change Canada, Burlington, ON, Canada.
  4. Vincent J Denef: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, United States of America.
  5. Michelle A Berry: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, United States of America.
  6. Gregory J Dick: Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, United States of America. ORCID

Abstract

Blooms of the potentially toxic cyanobacterium Microcystis are increasing worldwide. In the Laurentian Great Lakes they pose major socioeconomic, ecological, and human health threats, particularly in western Lake Erie. However, the interpretation of "omics" data is constrained by the highly variable genome of Microcystis and the small number of reference genome sequences from strains isolated from the Great Lakes. To address this, we sequenced two Microcystis isolates from Lake Erie (Microcystis aeruginosa LE3 and M. wesenbergii LE013-01) and one from upstream Lake St. Clair (M. cf aeruginosa LSC13-02), and compared these data to the genomes of seventeen Microcystis spp. from across the globe as well as one metagenome and seven metatranscriptomes from a 2014 Lake Erie Microcystis bloom. For the publically available strains analyzed, the core genome is ~1900 genes, representing ~11% of total genes in the pan-genome and ~45% of each strain's genome. The flexible genome content was related to Microcystis subclades defined by phylogenetic analysis of both housekeeping genes and total core genes. To our knowledge this is the first evidence that the flexible genome is linked to the core genome of the Microcystis species complex. The majority of strain-specific genes were present and expressed in bloom communities in Lake Erie. Roughly 8% of these genes from the lower Great Lakes are involved in genome plasticity (rapid gain, loss, or rearrangement of genes) and resistance to foreign genetic elements (such as CRISPR-Cas systems). Intriguingly, strain-specific genes from Microcystis cultured from around the world were also present and expressed in the Lake Erie blooms, suggesting that the Microcystis pangenome is truly global. The presence and expression of flexible genes, including strain-specific genes, suggests that strain-level genomic diversity may be important in maintaining Microcystis abundance during bloom events.

References

  1. Curr Protoc Bioinformatics. 2011 Sep;Chapter 6:6.12.1-6.12.19 [PMID: 21901743]
  2. Environ Microbiol. 2009 Apr;11(4):823-32 [PMID: 19021692]
  3. Adv Exp Med Biol. 2008;619:45-103 [PMID: 18461765]
  4. Microb Ecol. 2012 Jan;63(1):188-98 [PMID: 21720829]
  5. Bioinformatics. 2006 Nov 1;22(21):2688-90 [PMID: 16928733]
  6. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  7. Science. 2005 Aug 19;309(5738):1242-5 [PMID: 16109880]
  8. ISME J. 2009 Apr;3(4):419-29 [PMID: 19092863]
  9. Water Res. 2014 May 1;54:188-98 [PMID: 24568788]
  10. Bioinformatics. 2009 Jul 15;25(14):1754-60 [PMID: 19451168]
  11. BMC Genomics. 2008 Jun 05;9:274 [PMID: 18534010]
  12. ISME J. 2014 Oct;8(10):2080-92 [PMID: 24858783]
  13. Front Microbiol. 2015 Mar 19;6:219 [PMID: 25852675]
  14. Nucleic Acids Res. 2014 Jan;42(Database issue):D643-8 [PMID: 24293649]
  15. Appl Environ Microbiol. 2004 Jul;70(7):3979-87 [PMID: 15240273]
  16. Genome Announc. 2015 Mar 19;3(2): [PMID: 25792056]
  17. Appl Environ Microbiol. 2015 May 1;81(9):3268-76 [PMID: 25662977]
  18. Nucleic Acids Res. 2004 Feb 25;32(4):1363-71 [PMID: 14985472]
  19. Harmful Algae. 2016 Apr;54:223-238 [PMID: 28073479]
  20. Genome Biol. 2007;8(5):R71 [PMID: 17475002]
  21. Environ Sci Technol. 2017 Jun 20;51(12):6745-6755 [PMID: 28535339]
  22. Appl Environ Microbiol. 2012 Aug;78(15):5353-60 [PMID: 22636003]
  23. Proc Natl Acad Sci U S A. 2010 Feb 9;107(6):2383-90 [PMID: 20133593]
  24. PLoS One. 2014 Sep 10;9(9):e106093 [PMID: 25207941]
  25. Appl Environ Microbiol. 2013 Dec;79(24):7696-701 [PMID: 24096415]
  26. Science. 2014 Apr 25;344(6182):416-20 [PMID: 24763590]
  27. Neurotox Res. 2011 Apr;19(3):389-402 [PMID: 20376712]
  28. Environ Sci Technol. 2012 Mar 20;46(6):3480-8 [PMID: 22324444]
  29. Harmful Algae. 2016 Apr;54:4-20 [PMID: 28073480]
  30. PLoS One. 2013 Aug 12;8(8):e70747 [PMID: 23950996]
  31. PLoS One. 2011 Feb 24;6(2):e17085 [PMID: 21390221]
  32. Harmful Algae. 2016 Apr;54:87-97 [PMID: 28073483]
  33. Environ Microbiol. 2017 Mar;19(3):1149-1162 [PMID: 28026093]
  34. Trends Genet. 2013 Mar;29(3):170-5 [PMID: 23332119]
  35. Nature. 2011 Jun 29;474(7353):604-8 [PMID: 21720364]
  36. Nucleic Acids Res. 2017 Jan 4;45(D1):D507-D516 [PMID: 27738135]
  37. Bacteriol Rev. 1971 Jun;35(2):171-205 [PMID: 4998365]
  38. ISME J. 2015 Mar 17;9(4):909-21 [PMID: 25325384]
  39. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 [PMID: 23193283]
  40. Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13950-5 [PMID: 16172379]
  41. Environ Sci Technol. 2009 Jan 1;43(1):12-9 [PMID: 19209578]
  42. PLoS One. 2011 May 05;6(5):e19561 [PMID: 21573169]
  43. FEMS Microbiol Lett. 1999 Mar 1;172(1):15-21 [PMID: 10079523]
  44. Front Microbiol. 2015 May 12;6:394 [PMID: 26029174]
  45. PLoS Genet. 2007 Dec;3(12):e231 [PMID: 18159947]
  46. Appl Environ Microbiol. 2003 Sep;69(9):5716-21 [PMID: 12957969]
  47. Genome Biol. 2009;10(8):R85 [PMID: 19698104]
  48. Mol Biol Evol. 2013 Dec;30(12):2725-9 [PMID: 24132122]
  49. Science. 2008 May 23;320(5879):1081-5 [PMID: 18497299]
  50. Bioinformatics. 2012 Jun 1;28(11):1420-8 [PMID: 22495754]
  51. DNA Res. 2007 Dec 31;14(6):247-56 [PMID: 18192279]
  52. J Bacteriol. 2004 Apr;186(8):2355-65 [PMID: 15060038]
  53. PLoS One. 2013 Jul 23;8(7):e69834 [PMID: 23894552]
  54. ISME J. 2014 Mar;8(3):589-600 [PMID: 24132080]
  55. Genome Announc. 2013 Aug 01;1(4): [PMID: 23908289]
  56. Methods Mol Biol. 2015;1231:203-32 [PMID: 25343868]
  57. PLoS One. 2012;7(8):e42444 [PMID: 22870327]
  58. PLoS One. 2014 Jul 07;9(7):e101710 [PMID: 25000306]
  59. Bioinformatics. 2009 Sep 1;25(17):2271-8 [PMID: 19561336]
  60. Syst Biol. 2001 Aug;50(4):513-24 [PMID: 12116650]
  61. Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):568-73 [PMID: 14701903]
  62. BMC Bioinformatics. 2010 Mar 08;11:119 [PMID: 20211023]
  63. PeerJ. 2014 Jan 09;2:e243 [PMID: 24482762]
  64. Genome Biol. 2007;8(12):R267 [PMID: 18088402]
  65. PLoS One. 2013;8(2):e56470 [PMID: 23441196]
  66. Science. 2006 Mar 24;311(5768):1737-40 [PMID: 16556835]
  67. Harmful Algae. 2016 Apr;54:145-159 [PMID: 28073473]
  68. Microbiology (Reading). 2007 Nov;153(Pt 11):3695-3703 [PMID: 17975077]
  69. Science. 2008 Apr 4;320(5872):57-8 [PMID: 18388279]
  70. Microbiology (Reading). 2014 May;160(5):903-916 [PMID: 28206904]
  71. ISME J. 2010 Oct;4(10):1252-64 [PMID: 20463762]
  72. ISME J. 2016 Feb;10(2):333-45 [PMID: 26208139]
  73. J Mol Biol. 1990 Oct 5;215(3):403-10 [PMID: 2231712]
  74. Genome Res. 2002 Jul;12(7):1080-90 [PMID: 12097345]
  75. Nucleic Acids Res. 2014 Jan;42(Database issue):D568-73 [PMID: 24136997]
  76. Appl Environ Microbiol. 1984 Jan;47(1):49-55 [PMID: 6696422]
  77. Harmful Algae. 2016 May;55:97-111 [PMID: 28073551]
  78. Nucleic Acids Res. 2004 Mar 19;32(5):1792-7 [PMID: 15034147]
  79. Harmful Algae. 2016 Jun;56:44-66 [PMID: 28073496]
  80. Appl Environ Microbiol. 2001 Jun;67(6):2810-8 [PMID: 11375198]
  81. Nature. 1998 Jun 4;393(6684):464-7 [PMID: 9624000]
  82. Microbiol Mol Biol Rev. 2009 Jun;73(2):249-99 [PMID: 19487728]
  83. J Toxicol Environ Health B Crit Rev. 2005 Jan-Feb;8(1):1-37 [PMID: 15762553]
  84. J Phycol. 1968 Mar;4(1):1-4 [PMID: 27067764]
  85. Gene. 2011 Mar 1;473(2):139-49 [PMID: 21156198]

MeSH Term

Base Sequence
CRISPR-Cas Systems
Eutrophication
Gene Expression Regulation, Bacterial
Genes, Bacterial
Great Lakes Region
Metagenome
Microcystis
Phylogeny
Species Specificity

Word Cloud

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