Open Access
Issue
Published:
02 January 2021
Dramatic shifts in intestinal fungal community between wintering Hooded Crane and Domestic Goose
(
)
Download citation
768
Views
39
Downloads
9
Crossref
10
WoS
10
Scopus
0
CSCD
The intestinal microbiota play remarkable roles in maintaining the health of their hosts. Recent studies focused on gut bacterial diversity in birds and poultry, with little information about the ecological functions of their gut fungal community.
The high-throughput sequencing was applied to compare intestinal fungal community structure between Hooded Crane (Grus monacha) and Domestic Goose (Anser anser domesticus), and infer the potential pathogens of each species at Shengjin Lake of China.
Intestinal fungal alpha diversity was higher in Hooded Crane than Greylag Goose(Anser anser). Gut fungal community composition showed dramatic shifts between the two species. Hooded Cranes mainly eat Vallisneria natans and Potamogeton malaianus, while artificial hurl food (i.e., paddy) was the main food resource for Domestic Geese, suggesting that the variations in fungal community might be induced by different diets between the two hosts. Two enriched genera (i.e., Acremonium and Rhodotorula) which could increase host's digestion were detected in guts of Hooded Cranes. In addition, there were 42 pathogenic amplicon sequence variants (ASVs), 17% of which shared in Hooded Crane and Greylag Goose. The Hooded Crane had higher gut fungal pathogenic diversity and abundance relative to Greylag Goose.
The study demonstrated that divergence in intestinal fungal community structure might be induced by different diets between wintering Hooded Crane and Domestic Goose. Hooded Crane might rely more on their gut fungal taxa to acquire nutrients from indigestible food resources. Our study also implied that more research should focus on intestinal pathogens in wild birds and domestic poultry, as they might increase risk of disease in other animals, even human beings. The degree of cross infection in pathogens among wild birds and sympatric poultry should be clearly verified in future study.
menu
Dramatic shifts in intestinal fungal community between wintering Hooded Crane and Domestic Goose
(
)
Abstract
The intestinal microbiota play remarkable roles in maintaining the health of their hosts. Recent studies focused on gut bacterial diversity in birds and poultry, with little information about the ecological functions of their gut fungal community.
The high-throughput sequencing was applied to compare intestinal fungal community structure between Hooded Crane (Grus monacha) and Domestic Goose (Anser anser domesticus), and infer the potential pathogens of each species at Shengjin Lake of China.
Intestinal fungal alpha diversity was higher in Hooded Crane than Greylag Goose(Anser anser). Gut fungal community composition showed dramatic shifts between the two species. Hooded Cranes mainly eat Vallisneria natans and Potamogeton malaianus, while artificial hurl food (i.e., paddy) was the main food resource for Domestic Geese, suggesting that the variations in fungal community might be induced by different diets between the two hosts. Two enriched genera (i.e., Acremonium and Rhodotorula) which could increase host's digestion were detected in guts of Hooded Cranes. In addition, there were 42 pathogenic amplicon sequence variants (ASVs), 17% of which shared in Hooded Crane and Greylag Goose. The Hooded Crane had higher gut fungal pathogenic diversity and abundance relative to Greylag Goose.
The study demonstrated that divergence in intestinal fungal community structure might be induced by different diets between wintering Hooded Crane and Domestic Goose. Hooded Crane might rely more on their gut fungal taxa to acquire nutrients from indigestible food resources. Our study also implied that more research should focus on intestinal pathogens in wild birds and domestic poultry, as they might increase risk of disease in other animals, even human beings. The degree of cross infection in pathogens among wild birds and sympatric poultry should be clearly verified in future study.
References(41)
Alm EW, Daniels-Witt QR, Learman DR, Ryu H, Jordan DW, Gehring TM, et al. Potential for gulls to transport bacteria from human waste sites to beaches. Sci Total Environ. 2018;615: 123–30.
Altizer S, Bartel R, Han BA. Animal migration and infectious disease risk. Science. 2011;331: 296–302.
Amir A, McDonald D, Navas-Molina JA, Kopylova E, Morton JT, Xu ZZ, et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems. 2017;2: e00191-16.
Ayayee PA, Larsen T, Rosa C, Felton GW, Ferry JG, Hoover K. Essential amino acid supplementation by gut microbes of a wood-feeding cerambycid. Environ Entomol. 2016;45: 66–73.
Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E, Parks B, et al. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun. 2014;5: 4500.
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37: 1091.
Cafsi IE, Bjeoui S, Rabeh I, Nechi S. Effects of ochratoxin A on membrane phospholipids of the intestine of broiler chickens, practical consequences. Animal. 2020;14: 933–41.
Cantarel BL, Lombard V, Henrissat B. Complex carbohydrate utilization by the healthy human microbiome. PLoS ONE. 2012;7: e28742.
Chen M, Chen XQ, Tian LX, Liu YJ, Niu J. Enhanced intestinal health, immune responses and ammonia resistance in Pacific white shrimp (Litopenaeus vannamei) fed dietary hydrolyzed yeast (Rhodotorula mucilaginosa) and Bacillus licheniformi. Aquacult Rep. 2020;17: 100385.
Chung HC, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012;149: 1578–93.
Dong Y, Xiang X, Zhao G, Song Y, Zhou L. Variations in gut bacterial communities of Hooded Crane (Grus monacha) over spatial-temporal scales. PeerJ. 2019;7: e7045.
Eckburg P, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308: 1635–8.
Ekong PS, Fountain-Jones NM, Alkhamis MA. Spatiotemporal evolutionary epidemiology of H5N1 highly pathogenic avian influenza in West Africa and Nigeria, 2006–2015. Transbound Emerg Dis. 2018;65: 70–82.
Fox AD, Cao L, Zhang Y, Barter M, Zhao MJ, Meng FJ, et al. Declines in the tuber-feeding waterbird guild at Shengjin Lake National Nature Reserve, China—a barometer of submerged macrophyte collapse. Aquat Conserv. 2011;21: 82–91.
Fu R, Xiang XJ, Dong YQ, Cheng L, Zhou LZ. Comparing the intestinal bacterial communies of sympatric wintering Hooded Crane (Grus monacha) and Domestic Goose (Anser anser domesticus). Avian Res. 2020;11: 13.
Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE, Jimenez-Gasco MDM, et al. Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA. 2008;105: 12932–7.
Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM. Identification of birds through DNA barcodes. PLoS Biol. 2004;2: 1657–68.
Herr JR, Scully ED, Geib SM, Hoover K, Carlson JE, Geiser DM. Genome sequence of Fusarium isolate MYA-4552 from the midgut of Anoplophora glabripennis, an invasive, wood-boring beetle. Genome Announc. 2016;4: e00544-e616.
Li Y, Sun YK, Li X, Zhang GN, Xin HS, Xu HJ, et al. Effects of Acremonium terricola culture on performance, milk composition, rumen fermentation and immune functions in dairy cows. Anim Feed Sci Technol. 2018;240: 40–51.
Li Y, Zhang K, Liu Y, Li K, Hu D, Wronski T. Community composition and diversity of intestinal microbiota in captive and reintroduced Przewalski's horse (Equus ferus przewalskii). Front Microbiol. 2019;10: 1821.
Liu Y, Wang Y, Ni Y, Cheung CKY, Lam KSL, Wang Y, et al. Gut microbiome fermentation determines the efficacy of exercise for diabetes prevention. Cell Metab. 2020;31: 77–91.
Mason CJ, Campbell AM, Scully ED, Hoover K. Bacterial and fungal midgut community dynamics and transfer between mother and brood in the Asian Longhorned Beetle (Anoplophora glabripennis), an invasive xylophage. Microb Ecol. 2019;77: 230–42.
Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 2016;20: 241–8.
Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012;336: 1262–7.
Palamidi I, Mountzouris KC. Diet supplementation with an organic acids-based formulation affects gut microbiota and expression of gut barrier genes in broilers. Anim Nutr. 2018;4: 367–77.
Perofsky AC, Lewis RJ, Meyers LA. Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals. ISME J. 2019;13: 50–63.
Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555: 210–5.
Schmidt E, Mykytczuk N, Schulte-Hostedde AI. Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME J. 2019;13: 1293–305.
Scully ED, Hoover K, Carlson J, Tien M, Geib SM. Proteomic analysis of Fusarium solani isolated from the Asian longhorned beetle Anoplophora glabripennis. PLoS ONE. 2012;7: e32990.
Segata N, Izard J, Walron L, Gevers D, Miropolsky L, Garrett W, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12: R60.
Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA. 2010;107: 20051–6.
Singh P, Karmi A, Devendra K, Waldroup PW, Cho KK, Kwon YM. Influence of penicillin on microbial diversity of the cecal microbiota in broiler chickens. Poult Sci. 2013;92: 272–6.
Stanley D, Denman SE, Hughes RJ, Geier MS, Crowley TM, Chen H, et al. Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl Microbiol Biot. 2012;96: 1361–9.
Tanahashi M, Kubota K, Matsushita N, Togashi K. Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae). Naturwissenschaften. 2010;97: 311–7.
Tanahashi M, Kim JK, Watanabe K, Fukatsu T, Kubota K. Specificity and genetic diversity of xylose-fermenting Scheffersomyces yeasts associated with small blue stag beetles of the genus Platycerus in East Asia. Mycologia. 2017;109: 630–42.
Xiang XJ, Zhang FL, Fu R, Yan SF, Zhou LZ. Significant differences in bacterial and potentially pathogenic communities between sympatric Hooded Crane and Greater White-fronted Goose. Front Microbiol. 2019;10: 163.
Xu LT, Lu M, Xu DD, Chen L, Sun JH. Sexual variation of bacterial microbiota of Dendroctonus valens guts and frass in relation to verbenone production. J Insect Physiol. 2016;5: 110–7.
Yang L, Zhou L, Song Y. The effects of food abundance and disturbance on foraging flock patterns of the wintering Hooded Crane (Grus monacha). Avian Res. 2015;6: 15.
Zhang FL, Xiang XJ, Dong YQ, Yan SF, Song YW, Zhou LZ. Significant differences in the gut bacterial communities of Hooded Crane (Grus monacha) in different seasons at a stopover site on the flyway. Animals. 2020;10: 701.
Zhao YK, Liu JY, Liu JH, Lu S, Wu HH, Luo DQ. Recurrent Talaromyces marneffei infection presenting with intestinal obstruction in a patient with systemic lupus erythematosus. Mycopathologia. 2020;185: 717–26.
Zheng M, Zhou L, Zhao N, Xu W. Effects of variation in food resources on foraging habitat use by wintering Hooded Cranes (Grus monacha). Avian Res. 2015;6: 11.
Publication history
Copyright
Acknowledgements
We thank Mr. Wei Wang from Anhui University for assistance in sample collection, and Prof. Binghua Sun from Anhui University for assistance with manuscript revision.
Rights and permissions
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-sa/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
FEEDBACK 
TOP