California condor microbiomes: Bacterial variety and functional properties in captive-bred individuals

Autoři: Lindsey Jacobs aff001;  Benjamin H. McMahon aff001;  Joel Berendzen aff002;  Jonathan Longmire aff001;  Cheryl Gleasner aff001;  Nicolas W. Hengartner aff001;  Momchilo Vuyisich aff003;  Judith R. Cohn aff001;  Marti Jenkins aff004;  Andrew W. Bartlow aff001;  Jeanne M. Fair aff001
Působiště autorů: Los Alamos National Laboratory, Los Alamos, New Mexico, United States of America aff001;  GenerisBio, Santa Fe, New Mexico, United States of America aff002;  Viome, Los Alamos, New Mexico, United States of America aff003;  The Peregrine Fund, Boise, Idaho, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


Around the world, scavenging birds such as vultures and condors have been experiencing drastic population declines. Scavenging birds have a distinct digestive process to deal with higher amounts of bacteria in their primary diet of carcasses in varying levels of decay. These observations motivate us to present an analysis of captive and healthy California condor (Gymnogyps californianus) microbiomes to characterize a population raised together under similar conditions. Shotgun metagenomic DNA sequences were analyzed from fecal and cloacal samples of captive birds. Classification of shotgun DNA sequence data with peptide signatures using the Sequedex package provided both phylogenetic and functional profiles, as well as individually annotated reads for targeted confirmatory analysis. We observed bacterial species previously associated with birds and gut microbiomes, including both virulent and opportunistic pathogens such as Clostridium perfringens, Propionibacterium acnes, Shigella flexneri, and Fusobacterium mortiferum, common flora such as Lactobacillus johnsonii, Lactobacillus ruminus, and Bacteroides vulgatus, and mucosal microbes such as Delftia acidovorans, Stenotrophomonas maltophilia, and Corynebacterium falsnii. Classification using shotgun metagenomic reads from phylogenetic marker genes was consistent with, and more specific than, analysis based on 16S rDNA data. Classification of samples based on either phylogenetic or functional profiles of genomic fragments differentiated three types of samples: fecal, mature cloacal and immature cloacal, with immature birds having approximately 40% higher diversity of microbes.

Klíčová slova:

Animal phylogenetics – Bird genomics – Birds – Metagenomics – Microbiome – Phylogenetic analysis – RNA polymerase – Shotgun sequencing


1. Kelly TR, Rideout BA, Grantham J, Brandt J, Burnett LJ, Sorenson KJ, et al. Two decades of cumulative impacts to survivorship of endangered California condors in California. Biol Cons. 2015; 191:391–9. doi:

2. D’Elia J, Haig SM, Mullins TD, Miller MP Ancient DNA reveals substantial genetic diversity in the California Condor (Gymnogyps californianus) prior to a population bottleneck. Condor. 2016; 118:703–14. doi: 10.1650/condor-16-35.1

3. Straub MH, Kelly TR, Rideout BA, Eng C, Wynne J, Braun J, et al. Seroepidemiologic survey of potential pathogens in obligate and facultative scavenging avian species in California. PLoS ONE. 2015; 10:e0143018–e. doi: 10.1371/journal.pone.0143018 26606755

4. Waite DW, Taylor M Exploring the avian gut microbiota: current trends and future directions. Front Microbiol. 2015; 6. doi: 10.3389/fmicb.2015.00673 26191057

5. Waite DW, Taylor MW Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol. 2014; 5:223-. doi: 10.3389/fmicb.2014.00223 24904538

6. Teyssier A, Lens L, Matthysen E, White J Dynamics of gut microbiota diversity during the early development of an avian host: Evidence from a cross-foster experiment. Front Microbiol. 2018; 9. doi: 10.3389/fmicb.2018.01524 30038608

7. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, et al. Functional metagenomic profiling of nine biomes. Nature. 2008; 452:629–32. 18337718

8. Keenan SW, Engel AS, Elsey RM The alligator gut microbiome and implications for archosaur symbioses. Sci Reports. 2013; 3:2877. doi: 10.1038/srep02877 24096888

9. Wei S, Morrison M, Yu Z Bacterial census of poultry intestinal microbiome. Poultry Sci. 2013; 92:671–83. doi: 10.3382/ps.2012-02822 23436518

10. Waite DW, Deines P, Taylor MW Gut microbiome of the critically endangered New Zealand parrot, the Kakapo (Strigops habroptilus). PLoS ONE. 2012; 7:e35803–e. doi: 10.1371/journal.pone.0035803 22530070

11. Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J The microbiome of animals: implications for conservation biology. Internat J Genomics. 2016; 2016. doi: 10.1155/2016/5304028 27195280

12. Grond K, Sandercock BK, Jumpponen A, Zeglin LH The avian gut microbiota: community, physiology and function in wild birds. J Avian Biol. 2018; 49:e01788. doi: 10.1111/jav.01788

13. Borbón-García A, Reyes A, Vives-Flórez M, Caballero S Captivity shapes the gut microbiota of Andean bears: insights into health surveillance. Front Microbiol. 2017; 8:1316. doi: 10.3389/fmicb.2017.01316 28751883

14. Roggenbuck M, Bærholm Schnell I, Blom N, Bælum J, Bertelsen MF, Sicheritz-Pontén T, et al. The microbiome of New World vultures. Nature Comm. 2014; 5:5498 25423494

15. Marin C, Palomeque M, Marco-Jimenez F, Vega S Wild griffon vultures (Gyps fulvus) as a source of Salmonella and Cempylobacter in eastern Spain. PLoS ONE. 2004; 9:e9191. doi: 10.1371/journal.pone.0094191 24710464

16. Sulzner K, Kelly T, Smith W, Johnson CK Enteric pathogens and anitmicrobial resistence in turkey vultures (Cathartes aura) feeding at the wildlife-livestock interface. J Zoo Wildl Med. 2014; 45:931–4. doi: 10.1638/2012-0217.1 25632686

17. Houston DC, Cooper JE The digestive tract of the Whiteback Griffon vulture and its role in disease transmission among wild ungulates. J Wildl Dis. 1975; 11:306–13. doi: 10.7589/0090-3558-11.3.306 239254

18. Beasley DE, Koltz AM, Lambert JE, Fierer N, Dunn RR The evolution of stomach acidity and its relevance to the human microbiome. PLoS ONE. 2015; 10:e0134116–e. doi: 10.1371/journal.pone.0134116 26222383

19. Metcalf JL, Song SJ, Morton JT, Weiss S, Seguin-Orlando A, Joly F, et al. Evaluating the impact of domestication and captivity on the horse gut microbiome. Sci Reports. 2017; 7:15497. doi: 10.1038/s41598-017-15375-9 29138485

20. Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, et al. Captivity humanizes the primate microbiome. Proc Nat Acad Sci. 2016; 113:10376. doi: 10.1073/pnas.1521835113 27573830

21. McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, et al. The effects of captivity on the mammalian gut microbiome. Integrat Comp Biol. 2017; 57:690–704. doi: 10.1093/icb/icx090 28985326

22. Hird SM Evolutionary biology needs wild microbiomes. Front Microbiol. 2017; 8. doi: 10.3389/fmicb.2017.00725 28487687

23. Ballou AL, Ali RA, Mendoza MA, Ellis JC, Hassan HM, Croom WJ, et al. Development of the chick microbiome: how early exposure influences future microbial diversity. Front Vet Sci. 2016; 3. doi: 10.3389/fvets.2016.00002 26835461

24. Barbosa A, Balagué V, Valera F, Martínez A, Benzal J, Motas M, et al. Age-related differences in the gastrointestinal microbiota of chinstrap penguins (Pygoscelis antarctica). PLoS ONE. 2016; 11:e0153215–e. doi: 10.1371/journal.pone.0153215 27055030

25. Van Dogen WFD, White J, Brandl HB, Moodley Y, Merkling T, LeClaire S Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecology. 2013; 13. doi: 10.1186/1472-6785-13-11 23531085

26. Godoy-Vitorino F, Goldfarb KC, Brodie EL, Garcia-Amado MA, Michelangeli F, Dominguez M. G B Developmental microbial ecology of the crop of the folivorous hoatzin. ISME J. 2010; 4:611–20. doi: 10.1038/ismej.2009.147 20130656

27. Jovel J, Patterson J, Wang W, Hotte N, O’Keefe S, Mitchel T, et al. Characterization of the gut microbiome using 16S or shotgun metagenomics. Front Microbiol. 2016; 7:459. doi: 10.3389/fmicb.2016.00459 27148170

28. Berendzen J, Bruno William J, Cohn Judith D, Hengartner Nicolas W, Kuske Cheryl R, McMahon Benjamin H, et al. Rapid phylogenetic and functional classification of short genomic fragments with signature peptides. BMC Res Notes. 2012; 5:460-. doi: 10.1186/1756-0500-5-460 22925230

29. Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monog. 2014; 84:45–67. doi: 10.1890/13-0133.1

30. Hird SM, Sánchez C, Carstens BC, Brumfield RT Comparative gut microbiota of 59 neotropical bird species. Front Microbiol. 2015; 6. doi: 10.3389/fmicb.2015.01403 26733954

31. Vital M, Gao J, Rizzo M, Harrison T, Tiedje JM Diet is a major factor governing the fecal butyrate-producing community structure across Mammalia, Aves and Reptilia. The ISME J. 2014. doi: 10.1038/ismej.2014.179 25343515

32. Videvall E, Strandh M, Engelbrecht A, Cloete S, Cornwallis CK Measuring the gut microbiome in birds: Comparison of faecal and cloacal sampling. Molecul Ecol Resources. 2018; 18:424–34. doi: 10.1111/1755-0998.12744 29205893

33. Razzauti M, Galan M, Bernard M, Maman S, Klopp C, Charbonnel N, et al. Comparison between transcriptome sequencing and 16S metagenomics for detection of bacterial pathogens in wildlife. Plos Neglected Trop Dis. 2015; 9. doi: 10.1371/journal.pntd.0003929 26284930

34. Maeda I, Siddiki MSR, Nozawa-Takeda T, Tsukahara N, Tani Y, Naito T, et al. Population abundance of potentially pathogenic organisms in intestinal microbiome of Jungle Crow (Corvus macrorhynchos) shown with 16S rRNA gene-based microbial community analysis. BioMed Res Internat. 2013; 2013:5-. doi: 10.1155/2013/438956 24058905

35. Citron DM Update on the taxonomy and clinical aspects of the genus Fusobacterium. Clin Infect Dis. 2002; 35:S22–S7. doi: 10.1086/341916 12173104

36. Thompson J, Robrish SA, Bouma CL, Freedberg DI, Folk J Phospho-β-glucosidase from Fusobacterium mortiferum: Purification, cloning, and inactivation by 6-phosphoglucono-δ-lactone. J. Bacteriol. 1997; 179:1636–45. doi: 10.1128/jb.179.5.1636-1645.1997 9045824

37. Engevik M, Ganesh B, Morra C, Luk B, Versalovic J Modulation and adherence of intestinal mucus by commensal bacteria and the pathogen C. difficile. Faseb J. 2015; 29.

38. Barrionuevo M, Vullo D Bacterial swimming, swarming and chemotactic response to heavy metal presence: which could be the influence on wastewater biotreatment efficiency? World J Microbiol Biotech. 2012; 28:2813–25. doi: 10.1007/s11274-012-1091-5 22806721

39. Wu Y, Shukal S, Mukherjee M, Cao B Involvement in denitrification is beneficial to the biofilm lifestyle of Comamonas testosteroni: A mechanistic study and its environmental implications. Environ Sci Technol. 2015; 49:11551–9. doi: 10.1021/acs.est.5b03381 26327221

40. Kam S-K, Lee W-S, Ou T-Y, Teng S-O, Chen F-L Delftia acidovorans Bacteremia Associated with Ascending Urinary Tract Infections Proved by Molecular Method. J Exper Clin Med. 2012; 4:180–2. doi: 10.1016/j.jecm.2012.04.010

41. Wiley L, Odom JV, Bridge DR, Wiley LA, Elliott T, Olson JC Bacterial biofilm diversity in contact lens-related disease: Emerging role of Achromobacter, Stenotrophomonas, and Delftia. Invest Ophthalmol Visual Sci. 2012; 53:3896–905. doi: 10.1167/iovs.11-8762 22589441

42. Azevedo AS, Almeida C, Melo LF, Azevedo NF Interaction between atypical microorganisms and E. coli in catheter-associated urinary tract biofilms. Biofouling. 2014; 30:893–902. doi: 10.1080/08927014.2014.944173 25184430

43. Stanley D, Wu S-B, Rodgers N, Swick R, Moore R Differential responses of cecal microbiota to fishmeal, Eimeria and Clostridium perfringens in a necrotic enteritis challenge model in chickens. PLoS ONE. 2014; 9:e104739–e. doi: 10.1371/journal.pone.0104739 25167074

44. McDowell A, Barnard E, Nagy I, Gao A, Tomida S, Li H, et al. An expanded multilocus sequence typing scheme for Propionibacterium acnes: Investigation of ‘pathogenic’, ‘commensal’ and antibiotic resistant strains (expanded MLST for Propionibacterium acnes). Pos ONE. 2012; 7:e41480–e. doi: 10.1371/journal.pone.0041480 22859988

45. Cerdeño-Tárraga AM, Crossman LC, Lennard N, Harris B, Quail MA, Barron A, et al. Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science. 2005; 307:1463–5. doi: 10.1126/science.1107008 15746427

46. Ndamukong IC, Gee J, Smith JC The extracytoplasmic function sigma factor EcfO protects Bacteroides fragilis against oxidative stress. J Bacteriol. 2013; 195:145–55. doi: 10.1128/JB.01491-12 23104808

47. Galvão BPGV, Rafudeen MS, Abratt VR, Weber BW, Ferreira EO, Patrick S Identification of a collagen type I adhesin of Bacteroides fragilis. PLoS ONE. 2014; 9. doi: 10.1371/journal.pone.0091141 24618940

48. Saunders EH Complete genome sequence of Eggerthella lenta type strain (IPP VPI 0255T). Stand Genomic Sci. 2009; 1. doi: 10.4056/sigs.33592 21304654

49. Zychlinsky A, Prevost MC, Sansonetti PJ Shigella flexneri induces apoptosis in infected macrophages. Nature. 1992; 358:167–9. doi: 10.1038/358167a0 1614548

50. Sanada T, Kim M, Mimuro H, Suzuki M, Ogawa M, Oyama A, et al. The Shigella flexneri effector OspI deamidates UBC13 to dampen the inflammatory response. Nature. 2012; 483:623–6. doi: 10.1038/nature10894 22407319

51. Cai X, Zhang J, Chen M, Wu Y, Wang X, Chen J, et al. The effect of the potential PhoQ histidine kinase inhibitors on Shigella flexneri virulence. PLoS ONE. 2011; 6:e23100–e. doi: 10.1371/journal.pone.0023100 21853073

52. Rapport DJ, Hilden M An evolving role for ecological indicators: From documenting ecological conditions to monitoring drivers and policy responses. Ecol Indicators. 2013; 28:10–5. doi: 10.1016/j.ecolind.2012.05.015

53. Zhu SJ, Almagro-Garcia J, McVean G Deconvolution of multiple infections in Plasmodium falciparum from high throughput sequencing data. Bioinformatics. 2017; 34:9–15. doi: 10.1093/bioinformatics/btx530 28961721

54. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.4–4. 2017.

55. Team RC. A language and environment for statistical computing. R Foundation for Statistical Computing, R Foundation for Statistical Computing Vienna, Austria2017.

56. Caporaso JG, Justin K, Jesse S, Kyle B, Frederic DB, Elizabeth KC, et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods. 2010; 7:335-. doi: 10.1038/nmeth.f.303 20383131

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden