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Lemur Gut Microeukaryotic Community Variation Is Not Associated with Host Phylogeny, Diet, or Habitat

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Abstract

Identifying the major forces driving variation in gut microbiomes enhances our understanding of how and why symbioses between hosts and microbes evolved. Gut prokaryotic community variation is often closely associated with host evolutionary and ecological variables. Whether these same factors drive variation in other microbial taxa occupying the animal gut remains largely untested. Here, we present a one-to-one comparison of gut prokaryotic (16S rRNA metabarcoding) and microeukaryotic (18S rRNA metabarcoding) community patterning among 12 species of wild lemurs. Lemurs were sampled from dry forests and rainforests of southeastern Madagascar and display a range of phylogenetic and ecological niche diversity. We found that while lemur gut prokaryotic community diversity and composition vary with host taxonomy, diet, and habitat, gut microeukaryotic communities have no detectable association with any of these factors. We conclude that gut microeukaryotic community composition is largely random, while gut prokaryotic communities are conserved among host species. It is likely that a greater proportion of gut microeukaryotic communities comprise taxa with commensal, transient, and/or parasitic symbioses compared with gut prokaryotes, many of which form long-term relationships with the host and perform important biological functions. Our study highlights the importance of greater specificity in microbiome research; the gut microbiome contains many “omes” (e.g., prokaryome, eukaryome), each comprising different microbial taxa shaped by unique selective pressures.

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Data Availability

Data accessibility: 18S rRNA raw reads have been uploaded to the NCBI database (BioProject PRJNA913825) and will be released upon manuscript acceptance. 16S rRNA reads were published under NCBI BioProject PRJNA723621.

References

  1. Keeling PJ, del Campo J (2017) Marine protists are not just big bacteria. Curr. Biol. 27(11):R541–R549. https://doi.org/10.1016/j.cub.2017.03.075

    Article  CAS  PubMed  Google Scholar 

  2. Walker G, Dorrell RG, Schlacht A, Dacks JB (2011) Eukaryotic systematics: a user’s guide for cell biologists and parasitologists. Parasitology 138:1638–1663 10. 1017/S0031182010001708

    Article  PubMed  Google Scholar 

  3. Lukeš J, Stensvold CR, Jirku-Pomajbíková K, Parfrey LW (2015) Are human intestinal eukaryotes beneficial or commensals? PLoS Pathog. 11(8):e1005039. https://doi.org/10.1371/journal.ppat.1005039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Parfrey LW, Walters WA, Knight R (2011) Microbial eukaryotes in the human microbiome: ecology, evolution, and future directions. Front. Microbiol. 2. https://doi.org/10.3389/fmicb.2011.00153

  5. Radek R, Tischendorf G (1999) Bacterial adhesion to different termite flagellates: ultrastructural and function evidence for distinct molecular attachment modes. Protoplasma 207:43–53. https://doi.org/10.1007/BF01294712

    Article  CAS  Google Scholar 

  6. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292(5519):1115–1118. https://doi.org/10.1126/science.1058

    Article  CAS  PubMed  Google Scholar 

  7. Groussin M, Mazel F, Sanders JG, Smillie CS, Lavergne S, Thuiller W, Alm EJ (2017) Unraveling the processes shaping mammalian GMs over evolutionary time. Nat. Commun. 8:14319. https://doi.org/10.1038/ncomms14319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. de Mesquita CPB, Nichols LM, Gebert MJ, Vanderburgh C, Bocksberger G, Lester JD et al (2021) Structure of chimpanzee gut microbiomes across tropical Africa. mSystems 6(3). https://doi.org/10.1128/mSystems.01269-20

  9. Aivelo T, Medlar A, Löytynoja A, Laakkonen J, Jernvall J (2015) Tracking year-to-year changes in intestinal nematode communities of rufous mouse lemurs (Microcebus rufus). Parasitology 142(8):1095–1107. https://doi.org/10.1017/S0031182015000438

    Article  PubMed  Google Scholar 

  10. Murillo T, Schneider D, Fichtel C, Daniel R (2022) Dietary shifts and social interactions drive temporal fluctuations of the gut microbiome from wild redfronted lemurs. ISME Commun. 2:3. https://doi.org/10.1038/s43705-021-00086-0

    Article  PubMed Central  Google Scholar 

  11. Mann AE, Mazel F, Lamay MA, Morien E, Billy V, Kowalewski M et al (2020) Biodiversity of protists and nematodes in the wild nonhuman primate gut. ISME J. 14:609–622. https://doi.org/10.1038/s41396-019-0551-4

    Article  CAS  PubMed  Google Scholar 

  12. Amato KR, Sanders J, Song SJ, Nute M, Metcalf JL, Thompson LR, Leigh S (2019) Evolutionary trends in host physiology outweigh dietary niche in structuring primate GMs. ISME J. 13:576–587. https://doi.org/10.1038/s41396-018-0175-0

    Article  CAS  PubMed  Google Scholar 

  13. Everson KM, Pozzi LP, Barrett MA, Blair ME, Donohue ME, Kappeler PM et al (2023) Not one, but multiple radiations underlie the biodiversity of Madagascar's endangered lemurs. bioRxiv. https://doi.org/10.1101/2023.04.26.537867

  14. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb. Phys. Anthropol. 110(S29):31–72. https://doi.org/10.1002/(SICI)1096-8644(1999)110:29+<31::AID-AJPA3>3.0.CO;2-0

    Article  Google Scholar 

  15. Donohue ME, Rowe AK, Kowalewski E, Hert ZL, Karrick CE, Randriamanandaza LJ et al (2022) Significant effects of host dietary guild and phylogeny in wild lemur gut microbiomes. ISME Commun. 2:33. https://doi.org/10.1038/s43705-022-00115-6

    Article  PubMed Central  Google Scholar 

  16. Rowe AK, Donohue ME, Clare EL, Drinkwater R, Koenig A, Ridgway ZM, Martin LD, Nomenjanahary ES, Zakamanana F, Randriamananadaza LJ, Rakotonirina TE, Wright PC (2021) Exploratory analysis reveals arthropod consumption in 10 lemur species using DNA metabarcoding. Am. J. Primatol. 83(6):e23256. https://doi.org/10.1002/ajp.23256

    Article  CAS  PubMed  Google Scholar 

  17. Herrera JP, Dávalos L, M. (2016) Phylogeny and divergence times of lemurs inferred with recent and ancient fossils in the tree. Syst. Biol. 65:772–791. https://doi.org/10.1093/sysbio/syw035

    Article  PubMed  Google Scholar 

  18. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25:1965–1978. https://doi.org/10.1002/joc.1276

    Article  Google Scholar 

  19. Bradley IM, Pinto AJ, Guest JS (2016) Design and evaluation of Illumina MiSeq-compatible, 18S rRNA gene-specific primers for improved characterization of mixed phototrophic communities. Appl. Environ. Microbiol. 82(19). https://doi.org/10.1128/AEM.01630-16

  20. Vestheim H, Jarman SN (2008) Blocking primers to enhance PCR amplification of rare sequences in mixed samples – a case study on prey DNA in Antarctic krill stomachs. Front. Zool. 5:12. https://doi.org/10.1186/1742-9994-5-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. Peer J 4:e2584. https://doi.org/10.7717/peerj.2584

    Article  PubMed  PubMed Central  Google Scholar 

  22. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet C, Al-Ghalith GA et al (2019) QIIME2: reproducible, interactive, scalable, and extensive microbiome data science. Nat. Biotechnol. 37:852–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Quast C, Pruesse E, Yilmaz P, Gerkin J, Schweer T, Yarza P, Peplies J, Glöckner FO et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Nucleic Acids Res. 41(D1):D590–D596. https://doi.org/10.1093/nar/gks1219

  24. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinf. 10:421. https://doi.org/10.1186/1471-2105-10-421

    Article  CAS  Google Scholar 

  25. Mandal S, van Treuren W, White RA, Effesbø M, Knight R, Peddada SD (2015) Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb. Ecol. Health Dis. 26(1):27663. https://doi.org/10.3402/mehd.v26.27663

    Article  PubMed  Google Scholar 

  26. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS One 8(4):e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. GBIF Secretariat (2022). GBIF backbone taxonomy. Checklist dataset . https://doi.org/10.15468/39omei. Accessed 01 Jan 2021

  28. Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47(260):583–621. https://doi.org/10.1080/01621459.1952.10483441

    Article  Google Scholar 

  29. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  30. Blomberg SP, Garland T, Ives AR (2007) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745. https://doi.org/10.1111/j.00143820.2003.tb00285.x

    Article  Google Scholar 

  31. Harmon LJ, Weird JT, Brock CD, Glor RE, Challenger W (2007) GEIGER: investigating evolutionary radiations. Bioinformatics 24(1):129–131. https://doi.org/10.1093/bioinformatics/btm538

    Article  CAS  PubMed  Google Scholar 

  32. Harrell, F.E. (2020). Hmisc: Harrell miscellaneous. https://CRAN.R-project.org/package=Hmiscs

  33. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytopscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13:2498–2504. https://doi.org/10.1101/gr.1239303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Gerardo NM, Hoang KL, Stoy KS (2020) Evolution of animal immunity in the light of beneficial symbioses. Philos. Trans. R. Soc. B 375(1808). https://doi.org/10.1098/rstb.2019.0601

  35. Greene LK, Williams CV, Junge RE, Mahefarisoa KL, Rajaonarivelo T, Rakotondrainibe H, O’Connell TM, Drea CM (2020) A role for gut microbiota in host niche differentiation. ISME J. 14(7):1675–1687. https://doi.org/10.1038/s41396-020-0640-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordensten SR (2016) Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 14(11):e2000225. https://doi.org/10.1371/journal.pbio.2000225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. del Campo J, Bass D, Keeling PJ (2020) The eukaryome: diversity and role of microeukaryotic organisms associated with animal hosts. Funct. Ecol. 34:2045–2054. https://doi.org/10.1111/1365-2435.13490

    Article  Google Scholar 

  38. Greene LK, Bornbusch SL, McKenney EA, Harris RL, Gorvetzian SR, Yoder AD, Drea CM (2019) The importance of scale in comparative microbiome research: new insights from the gut and glands of captive and wild lemurs. Am. J. Primatol. 81(10-11):e22974. https://doi.org/10.1002/ajp.22974

    Article  PubMed  Google Scholar 

  39. Sauther ML, Cuozzo FP, Jacky IAY, Fish KD, LaFleur M, Ravelohasindrazana LAL, Ravoavy JF (2013) Limestone cliff-face and cave use by wild ring-tailed lemurs (Lemur catta) in southwestern Madagascar. Madagascar Conserv. Dev. 8(2):73–80. https://doi.org/10.4314/mcd.v8i2.5

    Article  Google Scholar 

  40. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS et al (2012) The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59(5):429–514. https://doi.org/10.1111/j.1550-7408.2012.00644.x

    Article  PubMed  PubMed Central  Google Scholar 

  41. Fernandes NM, Campello-Nunes PH, Paiva TS, Soares CAG, Silva-Neto I (2021) Ciliate diversity from aquatic environments in the Brazilian Atlantic Forest as revealed by high-throughput DNA sequencing. Microb. Ecol. 81:630–643. https://doi.org/10.1007/s00248-020-01612-8

    Article  PubMed  Google Scholar 

  42. Fierer N (2017) Embarcing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15(10):579–590. https://doi.org/10.1038/nrmicro.2017.87

    Article  CAS  PubMed  Google Scholar 

  43. Borruso L, Checcucchi A, Torti V, Correa F, Sandri C, Luise D et al (2021) I like the way you eat it: lemur (Indri indri) gut mycobiome and geophagy. Microb. Ecol. 82:215–223. https://doi.org/10.1007/s00248-020-01677-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hanson AM, Hodge KT, Porter LM (2003) Mycophagy among primates. Mycologist 17. https://doi.org/10.1017/S0269915X0300106X

  45. Findley K, Rodriguez-Carres M, Metin B, Kroiss J, Fonseca A, Vilgalys R, Heitman J (2009) Phylogeny and phenotypic characterization of pathogenic Cryptococcus species and closely related saprobic taxa in the Tremellales. Eukaryotic Cell 8(3). https://doi.org/10.1128/EC.00373-08

  46. Stark D, Barratt J, Chan D, Ellis JT (2016) Dientamoeba fragilis, the neglected trichomonad of the human bowel. Clin. Microbiol. Rev. 29(3):553–580. https://doi.org/10.1128/CMR.00076-15

    Article  PubMed  PubMed Central  Google Scholar 

  47. Inoue JI, Saita K, Kudo T, Ui S, Ohkuma M (2007) Hydrogen production by termit gut protists: characterization of iron hydrognases of parabasalian symbionts of the termite Coptotermes formosanus. Eukaryot. Cell 6(10). https://doi.org/10.1128/EC.00251-07

  48. Lima FS, Oikonomou G, Lima SF, Bicalho MLS, Ganda EK et al (2015) Prepartum and postpartum rumen fluid microbiomes: characterization and correlation with production traits in dairy cows. Applied. Environ. Microbiol. 81(4). https://doi.org/10.1128/AEM.03138-14

  49. Sharma AK, Davison S, Pafco B, Clayton JB, Rothman JM, McLennan MR, Cibot M, Fuh T, Vodicka R, Robinson CJ, Petrzelkova K, Gomez A (2022) The primate gut mycobiome-bacteriome interface is impacted by environmental and subsistence factors. Npj Biofilms Microbiomes 8:12. https://doi.org/10.1371/journal.ppat.1009253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Madagascar Ministry of Environment, Forests, and Ecology; and Madagascar National Parks in Andringitra National Park, Isalo National Park, Ranomafana National Park, and Zombitse-Vohibasia National Park for allowing us to conduct this field research. We thank Centre ValBio research station and MICET/ICTE for providing logistical support in Madagascar.

Funding

This work was supported by the following funders: the Animal Behaviour Society Student Research Grant; the American Society of Primatologists General Small Grant; the Global Wildlife Conservation’s Lemur Conservation Action Fund and IUCN’s Save Our Species (SOS); Grant-in-Aid of Research from Sigma Xi, The Scientific Research Society; HHMI Sustaining Excellence-2014 grant (#52008116), Primate Conservation, Inc.; Rowe-Wright Primate Fund; Society of Systematic Biologists Graduate Research Award; a Stony Brook University Graduate Student Employment Union Professional Development Award; a Stony Brook University Interdepartmental Doctoral Program in Anthropological Sciences Research Award; and the University of Kentucky Ribble Endowment Fund.

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Author notes

  1. Mariah E. Donohue, Zoe L. Hert, and Carly E. Karrick contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, University of Kentucky, 101 T.H.M. Building, Lexington, KY, 40506, USA

    Mariah E. Donohue, Zoe L. Hert, Carly E. Karrick, Kathryn M. Everson & David W. Weisrock

  2. Department of Biology, Indiana University, Bloomington, IN, USA

    Zoe L. Hert

  3. Department of BioSciences, Rice University, Houston, TX, USA

    Carly E. Karrick

  4. Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, New York, USA

    Amanda K. Rowe

  5. Department of Anthropology, Stony Brook University, Stony Brook, NY, USA

    Patricia C. Wright

  6. Centre ValBio Research Station, Ranomafana, MD, USA

    Patricia C. Wright, Lovasoa J. Randriamanandaza & François Zakamanana

  7. Anthropobiologie et Développement Durable, Université Antananarivo, Antananarivo, MD, USA

    Eva Stela Nomenjanahary

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Contributions

M. E. D., Z. L. H., C. E. K., and D. W. W. conceived and designed this study. M. E. D., A. K. R., L. J. R., F. Z., and S. N. collected samples. M. E. D, A. K. R., P. C. W., and D. W. W. contributed field equipment, facilities, and/or reagents. M. E. D., Z. L. H., and C. E. K. conducted laboratory work. M. E. D., Z. L. H., C. E. K., and K. M. E. analyzed the data. M. E. D., Z. L. H., and C. E. K. wrote the first draft of the manuscripts and all coauthors helped write and edit subsequent drafts.

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Correspondence to Mariah E. Donohue.

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Competing Interests

Patricia C. Wright is on the advisory board of Primate Conservation, Inc. (PCI), one of the funders of this project. She did not advise PCI on funding this project. All other authors declare no competing interests.

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Donohue, M.E., Hert, Z.L., Karrick, C.E. et al. Lemur Gut Microeukaryotic Community Variation Is Not Associated with Host Phylogeny, Diet, or Habitat. Microb Ecol 86, 2149–2160 (2023). https://doi.org/10.1007/s00248-023-02233-7

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