Fecal bacterial communities of the platypus (Ornithorhynchus anatinus) reflect captivity status – implications for conservation and management

The duck-billed platypus (Ornithorhynchus anatinus) is currently listed as ‘Near-Threatened’ under the International Union for Conservation of Nature (IUCN) Red List based on observed population declines and local extinctions. A key part of the conservation strategy for this species is its captive maintenance; however, captive animals often undergo significant changes in their gut microbiome. The study of the gut microbiome in threatened wildlife species has enormous potential to improve conservation efforts and gain insights into host-microbe coevolution. Here, for the first time, we characterize the gut microbiome of wild platypus via fecal samples using high-throughput sequencing of the bacterial 16S rRNA gene and identify microbial biomarkers of captivity in this species. At the phylum level, Firmicutes (50.4%) predominated among all platypuses, followed by Proteobacteria (28.7%), Fusobacteria (13.4%), and Bacteroidota (6.9%), with twenty-one ‘core’ bacteria identified. Captive individuals did not differ in their microbial α-diversity compared to wild platypus but had significantly different community composition (β-diversity) and exhibited higher abundances of Enterococcus, which are potential pathogenic bacteria. Four taxa were identified as biomarkers of wild platypus, including Rickettsiella, Epulopiscium, Clostridium, and Cetobacterium. This contrast in gut microbiome composition between wild and captive platypus is an essential insight for guiding conservation management as the rewilding of captive animal microbiomes is a new and emerging tool to improve captive animal health, maximize captive breeding efforts, and give reintroduced or translocated animals the best chance of survival.

[1]  J. Fenelon,et al.  Gut microbiota in the short‐beaked echidna (Tachyglossus Aculeatus) shows stability across gestation , 2023, MicrobiologyOpen.

[2]  R. V. Thurber,et al.  Horizon scanning the application of probiotics for wildlife. , 2023, Trends in microbiology.

[3]  Antton Alberdi,et al.  Mammals show distinct functional gut microbiome dynamics to identical series of environmental stressors , 2023, mBio.

[4]  V. McKenzie,et al.  Captivity, Reintroductions, and the Rewilding of Amphibian-associated Bacterial Communities , 2023, Microbial Ecology.

[5]  Guangchuang Yu,et al.  MicrobiotaProcess: A comprehensive R package for deep mining microbiome , 2023, Innovation (Cambridge (Mass.)).

[6]  R. Yue,et al.  Effects of captive and primate-focused tourism on the gut microbiome of Tibetan macaques , 2022, Frontiers in Microbiology.

[7]  L. Parfrey,et al.  Effects of captivity and rewilding on amphibian skin microbiomes , 2022, Biological Conservation.

[8]  Yang Cao,et al.  microbiomeMarker: an R/Bioconductor package for microbiome marker identification and visualization , 2022, Bioinform..

[9]  F. Grützner,et al.  Characterising the Gut Microbiomes in Wild and Captive Short-Beaked Echidnas Reveals Diet-Associated Changes , 2022, Frontiers in Microbiology.

[10]  Zhichao Zhou,et al.  Wild and Captive Environments Drive the Convergence of Gut Microbiota and Impact Health in Threatened Equids , 2022, Frontiers in Microbiology.

[11]  Xiaoting Yao,et al.  Intestinal Microbial Diversity of Free-Range and Captive Yak in Qinghai Province , 2022, Microorganisms.

[12]  J. J. McManus Didelphis virginiana , 2022, CABI Compendium.

[13]  L. Marinelli,et al.  Ornithorhynchus anatinus , 2022, CABI Compendium.

[14]  Dayong Li,et al.  Captivity Influences the Gut Microbiome of Rhinopithecus roxellana , 2021, Frontiers in Microbiology.

[15]  Honghai Zhang,et al.  Evolutionary and dietary relationships of wild mammals based on the gut microbiome. , 2021, Gene.

[16]  B. Cadiou,et al.  Comparative Analysis of Fecal Microbiomes From Wild Waterbirds to Poultry, Cattle, Pigs, and Wastewater Treatment Plants for a Microbial Source Tracking Approach , 2021, Frontiers in Microbiology.

[17]  A. Arnold,et al.  Vertically transmitted microbiome protects eggs from fungal infection and egg failure , 2021, Animal Microbiome.

[18]  Charlotte L. Oskam,et al.  Illuminating the bacterial microbiome of Australian ticks with 16S and Rickettsia-specific next-generation sequencing , 2021, Current research in parasitology & vector-borne diseases.

[19]  Fuhua Zhang,et al.  The gut microbiome of the Sunda pangolin (Manis javanica) reveals its adaptation to specialized myrmecophagy , 2021, PeerJ.

[20]  L. Blackall,et al.  Short-Term Exposure to Sterile Seawater Reduces Bacterial Community Diversity in the Sea Anemone, Exaiptasia diaphana , 2021, Frontiers in Marine Science.

[21]  C. Dickman,et al.  Platypus predation has differential effects on aquatic invertebrates in contrasting stream and lake ecosystems , 2020, Scientific Reports.

[22]  K. Whitehouse-Tedd,et al.  Integrating Gut Bacterial Diversity and Captive Husbandry to Optimize Vulture Conservation , 2020, Frontiers in Microbiology.

[23]  Brendan A. Wintle,et al.  A stitch in time – Synergistic impacts to platypus metapopulation extinction risk , 2020 .

[24]  S. Guo,et al.  Gut Microbiota of Wild and Captive Alpine Musk Deer (Moschus chrysogaster) , 2020, Frontiers in Microbiology.

[25]  R. Irizarry ggplot2 , 2019, Introduction to Data Science.

[26]  C. Grueber,et al.  Looking like the locals - gut microbiome changes post-release in an endangered species , 2019, Animal Microbiome.

[27]  Jack H. Pascoe,et al.  Faecal inoculations alter the gastrointestinal microbiome and allow dietary expansion in a wild specialist herbivore, the koala , 2019, Animal microbiome.

[28]  Francesco Asnicar,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[29]  W. Sherwin,et al.  The platypus: evolutionary history, biology, and an uncertain future , 2019, Journal of mammalogy.

[30]  B. Singh,et al.  The Koala (Phascolarctos cinereus) faecal microbiome differs with diet in a wild population , 2019, PeerJ.

[31]  K. Kohl,et al.  Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices , 2019, Proceedings of the Royal Society B.

[32]  R. Harris,et al.  Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine , 2018, Annals of the New York Academy of Sciences.

[33]  J. Webb,et al.  Cloacal and Ocular Microbiota of the Endangered Australian Northern Quoll , 2018, Microorganisms.

[34]  N. Mulder,et al.  Disruption of maternal gut microbiota during gestation alters offspring microbiota and immunity , 2018, Microbiome.

[35]  Benjamin D. Kaehler,et al.  Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin , 2018, Microbiome.

[36]  D. Relman,et al.  Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data , 2017, Microbiome.

[37]  B. Wachter,et al.  Gut microbiomes of free‐ranging and captive Namibian cheetahs: Diversity, putative functions and occurrence of potential pathogens , 2017, Molecular ecology.

[38]  U. Stingl,et al.  Genomic diversification of giant enteric symbionts reflects host dietary lifestyles , 2017, Proceedings of the National Academy of Sciences.

[39]  Alexander Lex,et al.  UpSetR: an R package for the visualization of intersecting sets and their properties , 2017, bioRxiv.

[40]  R. Knight,et al.  Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity , 2016, Proceedings of the Royal Society B: Biological Sciences.

[41]  Aaron W. Miller,et al.  Microbial Community Transplant Results in Increased and Long-Term Oxalate Degradation , 2016, Microbial Ecology.

[42]  F. Bäckhed,et al.  From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites , 2016, Cell.

[43]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[44]  D. Raoult,et al.  Detection of Bartonella tamiae, Coxiella burnetii and rickettsiae in arthropods and tissues from wild and domestic animals in northeastern Algeria , 2016, Parasites & Vectors.

[45]  A. Roca,et al.  Variation in koala microbiomes within and between individuals: effect of body region and captivity status , 2015, Scientific Reports.

[46]  Lawrence A. David,et al.  Diet rapidly and reproducibly alters the human gut microbiome , 2013, Nature.

[47]  A. Loudon,et al.  Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. , 2013, Ecology letters.

[48]  Mark V Brown,et al.  Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. , 2013, Environmental microbiology.

[49]  A. Knoll,et al.  Animals in a bacterial world, a new imperative for the life sciences , 2013, Proceedings of the National Academy of Sciences.

[50]  William A. Walters,et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms , 2012, The ISME Journal.

[51]  E. Pelletier,et al.  Clostridium sticklandii, a specialist in amino acid degradation:revisiting its metabolism through its genome sequence , 2010, BMC Genomics.

[52]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[53]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[54]  M. Hamady,et al.  Evolution of Mammals and Their Gut Microbes , 2008, Science.

[55]  E. Mardis,et al.  An obesity-associated gut microbiome with increased capacity for energy harvest , 2006, Nature.

[56]  S. Jackson,et al.  Reproductive behaviour and food consumption associated with the captive breeding of platypus (Ornithorhynchus anatinus) , 2002 .

[57]  M. Cheal Mammals , 1991, Experimental Gerontology.

[58]  Chaz Reetz-Laiolo Animals , 1981, Restoration & Management Notes.

[59]  Luca Paolini,et al.  Models , 2021, Encyclopedia of Gerontology and Population Aging.

[60]  Michael W Taylor,et al.  The microbiome in threatened species conservation , 2019, Biological Conservation.

[61]  H. Levkowitz,et al.  Reducing User Error by Establishing Encryption Patterns , 2011 .

[62]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[63]  Elizabeth Pike,et al.  Parable of the Platypus Dreaming , 1997 .

[64]  WG Co-chair,et al.  Animal Health , 1960, Nature.

[65]  J. Galloway A Review of the , 1901 .