Grey and Harbor Seals in France (mainland and Saint-Pierre Et Miquelon): Microbial Communities and Identification of a Microbial Source Tracking Seal Marker

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2024 Dec 19

PMID 39697652

Authors

Alisson Godino Sanchez

Joelle Serghine

Cecile Le Mennec

Cyril Noel

Julien Schaeffer

Herle Goraguer

Cecile Vincent

Thomas Vitre

Francoise S Le Guyader

Michele Gourmelon

Affiliations

Soon will be listed here.

Abstract

Introduction: Seals, protected wild marine mammals, are widely found in waters around the world. However, rising concerns about their increasing numbers in some areas have led to potential worries regarding microbiological contamination of coastal areas by their feces, which could impact bathing and shellfish-harvesting activities. To the best of our knowledge, no study has been conducted on the bacterial and RNA viral communities present in the feces of both grey and harbor seals, which are the two main seal species observed in mainland France and overseas.

Methods: Fecal bacterial ( = 132) and RNA viral ( = 40) communities of seals were analyzed using 16S rRNA gene amplicon high-throughput sequencing and viral RNA sequencing methods, respectively. In addition, to identify the specific characteristics of seal fecal microbial communities compared to other animal fecal microbial communities that may also contaminate coastal areas, the bacterial communities of seals were compared to those of wild waterbirds and breeding animals (i.e., cattle and pigs) which could be present in upstream catchments of coastal areas. Finally, ANCOM was used to identify unique and seal-associated Amplicon Sequence Variants (ASVs), aiming to develop a Microbial Source Tracking (MST) bacterial qPCR marker associated with seals.

Results And Discussion: The bacterial communities of grey and harbor seals were not found to be significantly different and were characterized by a predominance of Firmicutes, including the genera 1 and , followed by Fusobacteriota with the genus , and Bacteroidota with the genus . However, variations in bacterial communities between sites and individuals were observed. Similar observations were made for the RNA viral communities being characterized by a predominance of (44% of total reads) and (15%). This study successfully developed a sensitive (89.8%) and specific (97.1%) MST qPCR marker targeting grey seal-associated bacteria belonging to the Bifidobacteriaceae family. This marker can be used to identify potential fecal contamination of coastal areas by seals and complements the MST toolboxes of markers already developed for humans, wild birds and livestock.

References

Bik E, Costello E, Switzer A, Callahan B, Holmes S, Wells R . Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat Commun. 2016; 7:10516. PMC: 4742810. DOI: 10.1038/ncomms10516. View

Bergh O, Borsheim K, Bratbak G, Heldal M . High abundance of viruses found in aquatic environments. Nature. 1989; 340(6233):467-8. DOI: 10.1038/340467a0. View

Pacheco-Sandoval A, Lago-Leston A, Abadia-Cardoso A, Solana-Arellano E, Schramm Y . Age as a primary driver of the gut microbial composition and function in wild harbor seals. Sci Rep. 2022; 12(1):14641. PMC: 9420123. DOI: 10.1038/s41598-022-18565-2. View

Bennett K, Eley A . Fusobacteria: new taxonomy and related diseases. J Med Microbiol. 1993; 39(4):246-54. DOI: 10.1099/00222615-39-4-246. View

Hughes S, Greig D, Miller W, Byrne B, Gulland F, Harvey J . Dynamics of Vibrio with virulence genes detected in Pacific harbor seals (Phoca vitulina richardii) off California: implications for marine mammal health. Microb Ecol. 2013; 65(4):982-94. DOI: 10.1007/s00248-013-0188-1. View

Baily J, Meric G, Bayliss S, Foster G, Moss S, Watson E . Evidence of land-sea transfer of the zoonotic pathogen Campylobacter to a wildlife marine sentinel species. Mol Ecol. 2014; 24(1):208-21. DOI: 10.1111/mec.13001. View

Lozupone C, Lladser M, Knights D, Stombaugh J, Knight R . UniFrac: an effective distance metric for microbial community comparison. ISME J. 2010; 5(2):169-72. PMC: 3105689. DOI: 10.1038/ismej.2010.133. View

Bonny P, Schaeffer J, Besnard A, Desdouits M, Ngang J, Le Guyader F . Human and Animal RNA Virus Diversity Detected by Metagenomics in Cameroonian Clams. Front Microbiol. 2021; 12:770385. PMC: 8669915. DOI: 10.3389/fmicb.2021.770385. View

Gourmelon M, Caprais M, Mieszkin S, Marti R, Wery N, Jarde E . Development of microbial and chemical MST tools to identify the origin of the faecal pollution in bathing and shellfish harvesting waters in France. Water Res. 2010; 44(16):4812-24. DOI: 10.1016/j.watres.2010.07.061. View

10.

Jarde E, Jeanneau L, Harrault L, Quenot E, Solecki O, Petitjean P . Application of a microbial source tracking based on bacterial and chemical markers in headwater and coastal catchments. Sci Total Environ. 2017; 610-611:55-63. DOI: 10.1016/j.scitotenv.2017.07.235. View

11.

Pacheco-Sandoval A, Schramm Y, Heckel G, Giffard-Mena I, Lago-Leston A . Unraveling the gut microbiota of Mexican pinnipeds: the dominance of life histories over phylogeny. Appl Environ Microbiol. 2024; 90(6):e0203023. PMC: 11218648. DOI: 10.1128/aem.02030-23. View

12.

Berg M, Forberg K, Perez L, Luk K, Meyer T, Cloherty G . Emergence of a Distinct Picobirnavirus Genotype Circulating in Patients Hospitalized with Acute Respiratory Illness. Viruses. 2021; 13(12). PMC: 8708096. DOI: 10.3390/v13122534. View

13.

Paar 3rd J, Willis J, Sette L, Wood S, Bogomolni A, Dulac M . Occurrence of recreational water quality monitoring general fecal indicator bacteria and fecal source identification genetic markers in gray seal scat. Sci Total Environ. 2024; 934:173220. DOI: 10.1016/j.scitotenv.2024.173220. View

14.

Sunagawa S, Acinas S, Bork P, Bowler C, Eveillard D, Gorsky G . Tara Oceans: towards global ocean ecosystems biology. Nat Rev Microbiol. 2020; 18(8):428-445. DOI: 10.1038/s41579-020-0364-5. View

15.

Sinigalliano C, Kim K, Gidley M, Yuknavage K, Knee K, Palacios D . Microbial Source Tracking of Fecal Indicating Bacteria in Coral Reef Waters, Recreational Waters, and Groundwater of Saipan by Real-Time Quantitative PCR. Front Microbiol. 2021; 11:596650. PMC: 7848096. DOI: 10.3389/fmicb.2020.596650. View

16.

Ley R, Hamady M, Lozupone C, Turnbaugh P, Ramey R, Bircher J . Evolution of mammals and their gut microbes. Science. 2008; 320(5883):1647-51. PMC: 2649005. DOI: 10.1126/science.1155725. View

17.

Glockner F, Yilmaz P, Quast C, Gerken J, Beccati A, Ciuprina A . 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol. 2017; 261:169-176. DOI: 10.1016/j.jbiotec.2017.06.1198. View

18.

Mieszkin S, Furet J, Corthier G, Gourmelon M . Estimation of pig fecal contamination in a river catchment by real-time PCR using two pig-specific Bacteroidales 16S rRNA genetic markers. Appl Environ Microbiol. 2009; 75(10):3045-54. PMC: 2681621. DOI: 10.1128/AEM.02343-08. View

19.

Greig D, Gulland F, Smith W, Conrad P, Field C, Fleetwood M . Surveillance for zoonotic and selected pathogens in harbor seals Phoca vitulina from central California. Dis Aquat Organ. 2014; 111(2):93-106. DOI: 10.3354/dao02762. View

20.

Callahan B, McMurdie P, Rosen M, Han A, Johnson A, Holmes S . DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016; 13(7):581-3. PMC: 4927377. DOI: 10.1038/nmeth.3869. View