High-resolution genomic analysis to investigate the impact of the invasive brushtail possum (Trichosurus vulpecula) and other wildlife on microbial water quality assessments.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101285081 Publication Model: eCollection Cited Medium: Internet ISSN: 1932-6203 (Electronic) Linking ISSN: 19326203 NLM ISO Abbreviation: PLoS One Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science

Animals, Wild* ; Trichosurus*/genetics; Animals ; Humans ; Water Quality ; Ecosystem ; Phylogeny ; Escherichia coli/genetics ; Genomics ; New Zealand

Escherichia coli are routine indicators of fecal contamination in water quality assessments. Contrary to livestock and human activities, brushtail possums (Trichosurus vulpecula), common invasive marsupials in Aotearoa/New Zealand, have not been thoroughly studied as a source of fecal contamination in freshwater. To investigate their potential role, Escherichia spp. isolates (n = 420) were recovered from possum gut contents and feces and were compared to those from water, soil, sediment, and periphyton samples, and from birds and other introduced mammals collected within the Mākirikiri Reserve, Dannevirke. Isolates were characterized using E. coli-specific real-time PCR targeting the uidA gene, Sanger sequencing of a partial gnd PCR product to generate a gnd sequence type (gST), and for 101 isolates, whole genome sequencing. Escherichia populations from 106 animal and environmental sample enrichments were analyzed using gnd metabarcoding. The alpha diversity of Escherichia gSTs was significantly lower in possums and animals compared with aquatic environmental samples, and some gSTs were shared between sample types, e.g., gST535 (in 85% of samples) and gST258 (71%). Forty percent of isolates gnd-typed and 75% of reads obtained by metabarcoding had gSTs shared between possums, other animals, and the environment. Core-genome single nucleotide polymorphism (SNP) analysis showed limited variation between several animal and environmental isolates (<10 SNPs). Our data show at an unprecedented scale that Escherichia clones are shared between possums, other wildlife, water, and the wider environment. These findings support the potential role of possums as contributors to fecal contamination in Aotearoa/New Zealand freshwater. Our study deepens the current knowledge of Escherichia populations in under-sampled wildlife. It presents a successful application of high-resolution genomic methods for fecal source tracking, thereby broadening the analytical toolbox available to water quality managers. Phylogenetic analysis of isolates and profiling of Escherichia populations provided useful information on the source(s) of fecal contamination and suggest that comprehensive invasive species management strategies may assist in restoring not only ecosystem health but also water health where microbial water quality is compromised.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Moinet et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

J Appl Microbiol. 2005;99(2):301-9. (PMID: 16033461)
Genome Biol. 2018 Oct 4;19(1):153. (PMID: 30286803)
J Med Microbiol. 2007 May;56(Pt 5):620-628. (PMID: 17446284)
Environ Microbiol. 2013 Aug;15(8):2162-72. (PMID: 23414000)
Environ Microbiol. 2011 Sep;13(9):2468-77. (PMID: 21651689)
Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10227-31. (PMID: 7937867)
J Appl Microbiol. 2017 Sep;123(3):570-581. (PMID: 28383815)
Int J Syst Evol Microbiol. 2015 Jul;65(7):2130-2134. (PMID: 25851592)
EcoSal Plus. 2015;6(2):. (PMID: 26435255)
Appl Environ Microbiol. 2012 Jan;78(2):503-10. (PMID: 22081573)
Sci Rep. 2017 Apr 12;7(1):841. (PMID: 28404985)
PLoS Comput Biol. 2014 Apr 03;10(4):e1003531. (PMID: 24699258)
Water Res. 2018 Nov 1;144:424-434. (PMID: 30059905)
BMC Bioinformatics. 2010 Dec 10;11:595. (PMID: 21143983)
PeerJ. 2022 Mar 1;10:e12935. (PMID: 35251780)
Microbiol Resour Announc. 2019 Nov 21;8(47):. (PMID: 31753948)
Nat Methods. 2016 Jul;13(7):581-3. (PMID: 27214047)
PLoS One. 2013 Apr 22;8(4):e61217. (PMID: 23630581)
Microbiol Resour Announc. 2019 Aug 15;8(33):. (PMID: 31416858)
Bioinformatics. 2014 Aug 1;30(15):2114-20. (PMID: 24695404)
PeerJ. 2021 Apr 06;9:e10941. (PMID: 33868800)
Microb Genom. 2022 Oct;8(10):. (PMID: 36200854)
J Water Health. 2013 Sep;11(3):397-409. (PMID: 23981869)
Appl Environ Microbiol. 2009 Oct;75(20):6534-44. (PMID: 19700542)
Infect Immun. 2012 Dec;80(12):4115-22. (PMID: 22966046)
J Med Microbiol. 2009 Jul;58(Pt 7):905-911. (PMID: 19502373)
BMC Microbiol. 2014 Apr 28;14:109. (PMID: 24774171)
Curr Res Microb Sci. 2021 Dec 20;3:100093. (PMID: 35005658)
Genetics. 2003 Feb;163(2):475-83. (PMID: 12618387)
Microb Genom. 2018 Jul;4(7):. (PMID: 29916797)
J Microbiol Methods. 2016 Oct;129:85-93. (PMID: 27432340)
Appl Environ Microbiol. 2022 May 10;88(9):e0027722. (PMID: 35442082)
Biostatistics. 2022 Jan 13;23(1):207-222. (PMID: 32432696)
J Sci Food Agric. 1977 Sep;28(9):829-32. (PMID: 198612)
J Clin Microbiol. 2020 Sep 22;58(10):. (PMID: 32669379)
Emerg Infect Dis. 2019 Mar;25(3):489-500. (PMID: 30789138)
Genome Res. 2020 Jan;30(1):138-152. (PMID: 31809257)
Int J Syst Evol Microbiol. 2021 Feb;71(2):. (PMID: 33406029)
Science. 1980 Oct 31;210(4469):545-7. (PMID: 6999623)
J Environ Manage. 2018 Sep 15;222:293-303. (PMID: 29860123)
Sci Total Environ. 2022 Nov 20;848:157741. (PMID: 35917960)
J Food Prot. 2012 Apr;75(4):643-50. (PMID: 22488051)
J Bacteriol. 2000 Nov;182(21):6183-91. (PMID: 11029441)
Antimicrob Agents Chemother. 2019 Oct 22;63(11):. (PMID: 31427293)
Appl Environ Microbiol. 2016 Jun 30;82(14):4379-4386. (PMID: 27208100)
Water Res. 2020 Oct 15;185:116204. (PMID: 32745743)
Vet Microbiol. 2011 Jul 5;151(1-2):34-42. (PMID: 21458931)
Nucleic Acids Res. 2019 Jan 8;47(D1):D687-D692. (PMID: 30395255)
Front Microbiol. 2019 Oct 23;10:2407. (PMID: 31708888)
Appl Environ Microbiol. 2015 Aug;81(15):5123-33. (PMID: 26002899)
Proc Biol Sci. 2021 Apr 14;288(1948):20210399. (PMID: 33849316)
Environ Sci Technol. 2015 Aug 4;49(15):9341-6. (PMID: 26151092)
Genome Biol. 2016 Jun 20;17(1):132. (PMID: 27323842)
Genome Announc. 2018 May 3;6(18):. (PMID: 29724828)
Bioinformatics. 2014 Jul 15;30(14):2068-9. (PMID: 24642063)
Appl Environ Microbiol. 2023 Jun 28;89(6):e0014223. (PMID: 37191541)
Commun Biol. 2021 Jan 26;4(1):117. (PMID: 33500552)
Appl Environ Microbiol. 2019 Nov 27;85(24):. (PMID: 31562175)
Microb Genom. 2021 Dec;7(12):. (PMID: 34860150)

Date Created: 20240118 Date Completed: 20240122 Latest Revision: 20240201

20250114

PMC10796070

10.1371/journal.pone.0295529

38236841