Temporal Stability and the Effect of Transgenerational Transfer on Fecal Microbiota Structure in a Long Distance Migratory Bird
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
28220109
PubMed Central
PMC5292904
DOI
10.3389/fmicb.2017.00050
Knihovny.cz E-resources
- Keywords
- barn swallow, fecal microbiota, gastrointestinal tract, metagenome, microbiome, symbiosis,
- Publication type
- Journal Article MeSH
Animal bodies are inhabited by a taxonomically and functionally diverse community of symbiotic and commensal microorganisms. From an ecological and evolutionary perspective, inter-individual variation in host-associated microbiota contributes to physiological and immune system variation. As such, host-associated microbiota may be considered an integral part of the host's phenotype, serving as a substrate for natural selection. This assumes that host-associated microbiota exhibits high temporal stability, however, and that its composition is shaped by trans-generational transfer or heritable host-associated microbiota modulators encoded by the host genome. Although this concept is widely accepted, its crucial assumptions have rarely been tested in wild vertebrate populations. We performed 16S rRNA metabarcoding on an extensive set of fecal microbiota (FM) samples from an insectivorous, long-distance migratory bird, the barn swallow (Hirundo rustica). Our data revealed clear differences in FM among juveniles and adults as regards taxonomic and functional composition, diversity and co-occurrence network complexity. Multiple FM samples from the same juvenile or adult collected within single breeding seasons exhibited higher similarity than expected by chance, as did adult FM samples over two consecutive years. Despite low effect sizes for FM stability over time at the community level, we identified an adult FM subset with relative abundances exhibiting significant temporal consistency, possibly inducing long-term effects on the host phenotype. Our data also indicate a slight maternal (but not paternal) effect on FM composition in social offspring, though this is unlikely to persist into adulthood. We discuss our findings in the context of both evolution and ecology of microbiota vs. host interactions and barn swallow biology.
Department of Ecology Faculty of Science Charles University Prague Czechia
Department of Zoology Faculty of Science Charles University Prague Czechia
Institute of Vertebrate Biology Czech Academy of Sciences Studenec Czechia
See more in PubMed
Abe F., Ishibashi N., Shimamura S. (1995). Effect of administration of bifidobacteria and lactic acid bacteria to newborn calves and piglets. PubMed DOI
Amato K. R. (2013). Co-evolution in context: the importance of studying gut microbiomes in wild animals. DOI
Amato K. R., Yeoman C. J., Kent A., Righini N., Carbonero F., Estrada A., et al. (2013). Habitat degradation impacts black howler monkey ( PubMed DOI PMC
Askarian F., Zhou Z., Olsen R. E., Sperstad S., Ringø E. (2012). Culturable autochthonous gut bacteria in Atlantic salmon ( DOI
Bäckhed F., Ley R. E., Sonnenburg J. L., Peterson D. A., Gordon J. I. (2005). Host-bacterial mutualism in the human intestine. PubMed DOI
Bäckhed F., Roswall J., Peng Y., Feng Q., Jia H., Kovatcheva-Datchary P., et al. (2015). Dynamics and stabilization of the human gut microbiome during the first year of life. PubMed DOI
Bates D., Mächler M., Bolker B., Walker S. (2015). Fitting linear mixed-effects models using lme4. DOI
Baxter N. T., Wan J. J., Schubert A. M., Jenior M. L., Myers P., Schloss P. D. (2015). Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric PubMed DOI PMC
Becker A. A. M. J., Janssens G. P. J., Snauwaert C., Hesta M., Huys G. (2015). Integrated community profiling indicates long-term temporal stability of the predominant faecal microbiota in captive cheetahs. PubMed DOI PMC
Bennett P., Owens I. (2002).
Benskin C. M. H., Rhodes G., Pickup R. W., Mainwaring M. C., Wilson K., Hartley I. R. (2015). Life history correlates of fecal bacterial species richness in a wild population of the blue tit PubMed DOI PMC
Benskin C. M. H., Rhodes G., Pickup R. W., Wilson K., Hartley I. R. (2010). Diversity and temporal stability of bacterial communities in a model passerine bird, the zebra finch. PubMed DOI
Benson A. K., Kelly S. A., Legge R., Ma F., Low S. J., Kim J., et al. (2010). Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PubMed DOI PMC
Bode L. (2012). Human milk oligosaccharides: every baby needs a sugar mama PubMed DOI PMC
Bolnick D. I., Snowberg L. K., Caporaso J. G., Lauber C., Knight R., Stutz W. E. (2014). Major histocompatibility complex class IIb polymorphism influences gut microbiota composition and diversity. PubMed DOI
Bordenstein S. R., Theis K. R. (2015). Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PubMed DOI PMC
Borland S. E., Robinson S. M., Crozier S. R., Inskip H. M. (2007). Stability of dietary patterns in young women over a 2-year period. PubMed DOI
Bourgon R., Gentleman R., Huber W. (2010). Independent filtering increases detection power for high-throughput experiments. PubMed DOI PMC
Boutin S., Bernatchez L., Audet C., Derôme N. (2012). Antagonistic effect of indigenous skin bacteria of brook charr ( PubMed DOI
Braun E. J., Campbell C. E. (1989). Uric acid decomposition in the lower gastrointestinal tract. PubMed DOI
Brucker R. M., Bordenstein S. R. (2012). Speciation by symbiosis. PubMed DOI
Caporaso J. G., Bittinger K., Bushman F. D., DeSantis T. Z., Andersen G. L., Knight R. (2010a). PyNAST: a flexible tool for aligning sequences to a template alignment. PubMed DOI PMC
Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. (2010b). QIIME allows analysis of high-throughput community sequencing data. PubMed DOI PMC
Caviedes-Vidal E., Karasov W. H. (2001). Developmental changes in digestive physiology of nestling house sparrows, PubMed DOI
Caviedes-Vidal E., McWhorter T. J., Lavin S. R., Chediack J. G., Tracy C. R., Karasov W. H. (2007). The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. PubMed DOI PMC
Chu H. W., Honour J. M., Rawlinson C. A., Harbeck R. J., Martin R. J. (2003). Effects of respiratory PubMed DOI PMC
Correa N. B. O., Peret Filho L. A., Penna F. J., Lima F. M. L. S., Nicoli J. R. (2005). A randomized formula controlled trial of PubMed DOI
Costea P. I., Lundeberg J., Akan P. (2013). TagGD: fast and accurate software for DNA Tag generation and demultiplexing. PubMed DOI PMC
Dapito D. H., Mencin A., Gwak G.-Y., Pradere J.-P., Jang M.-K., Mederacke I., et al. (2012). Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. PubMed DOI PMC
David L. A., Maurice C. F., Carmody R. N., Gootenberg D. B., Button J. E., Wolfe B. E., et al. (2014). Diet rapidly and reproducibly alters the human gut microbiome. PubMed DOI PMC
den Besten G., van Eunen K., Groen A. K., Venema K., Reijngoud D.-J., Bakker B. M. (2013). The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. PubMed DOI PMC
DeSantis T. Z., Hugenholtz P., Larsen N., Rojas M., Brodie E. L., Keller K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. PubMed DOI PMC
DiBaise J. K., Frank D. N., Mathur R. (2012). Impact of the gut microbiota on the development of obesity: current concepts. DOI
Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. PubMed DOI
Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. PubMed DOI PMC
Edstrom K. M., Devine C. M. (2001). Consistency in women’s orientations to food and nutrition in midlife and older age: a 10-year qualitative follow-up. PubMed DOI
Epskamp S., Cramer A. O. J., Waldorp L. J., Schmittmann V. D., Borsboom D. (2012). Qgraph: network visualizations of relationships in psychometric data. DOI
Faith J. J., Guruge J. L., Charbonneau M., Subramanian S., Seedorf H., Goodman A. L., et al. (2013). The long-term stability of the human gut microbiota. PubMed DOI PMC
Falush D., Wirth T., Linz B., Pritchard J. K., Stephens M., Kidd M., et al. (2003). Traces of human migrations in PubMed DOI
Faust K., Sathirapongsasuti J. F., Izard J., Segata N., Gevers D., Raes J., et al. (2012). Microbial co-occurrence relationships in the human microbiome. PubMed DOI PMC
Funkhouser L. J., Bordenstein S. R. (2013). Mom knows best: the universality of maternal microbial transmission. PubMed DOI PMC
Garamszegi L. Z., Eens M., Hurtrez-Boussès S., Møller A. P. (2005). Testosterone, testes size, and mating success in birds: a comparative study. PubMed DOI
González-Braojos S., Vela A. I., Ruiz-De-Castañeda R., Briones V., Cantarero A., Moreno J. (2012a). Is nestling growth affected by nest reuse and skin bacteria in Pied Flycatchers DOI
González-Braojos S., Vela A. I., Ruiz-de-Castañeda R., Briones V., Moreno J. (2012b). Age-related changes in abundance of enterococci and DOI
Harbour S., Sutton P. (2008). Immunogenicity and pathogenicity of PubMed DOI
Hildebrand F., Tadeo R., Voigt A. Y., Bork P., Raes J. (2014). LotuS: an efficient and user-friendly OTU processing pipeline. PubMed DOI PMC
Hird S. M., Sánchez C., Carstens B. C., Brumfield R. T. (2015). Comparative gut microbiota of 59 neotropical bird species. PubMed DOI PMC
Hoy Y. E., Bik E. M., Lawley T. D., Holmes S. P., Monack D. M., Theriot J. A., et al. (2015). Variation in taxonomic composition of the fecal microbiota in an inbred mouse strain across individuals and time. PubMed DOI PMC
Janson E. M., Stireman J. O., Singer M. S., Abbot P. (2008). Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. PubMed DOI
Jumpertz R., Le D. S., Turnbaugh P. J., Trinidad C., Bogardus C., Gordon J. I., et al. (2011). Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. PubMed DOI PMC
Kandler O. (1983). Carbohydrate metabolism in lactic acid bacteria. PubMed DOI
Kanehisa M., Goto S. (2000). KEGG: kyoto encyclopedia of genes and genomes. PubMed DOI PMC
Karasov W. H. (1990). Digestion in birds: chemical and physiological determinants and ecological implications.
Killpack T. L., Oguchi Y., Karasov W. H. (2013). Ontogenetic patterns of constitutive immune parameters in altricial house sparrows. DOI
Kirkwood J. K., Macgregor S. K., Malnick H., Foster G. (2006). Unusual mortality incidents in tit species (family Paridae) associated with the novel bacterium PubMed DOI
Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., et al. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. PubMed DOI PMC
Koch H., Schmid-Hempel P. (2011). Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. PubMed DOI PMC
Koren O., Goodrich J. K., Cullender T. C., Spor A., Laitinen K., Bäckhed H. K., et al. (2012). Host remodeling of the gut microbiome and metabolic changes during pregnancy. PubMed DOI PMC
Kreisinger J., Bastien G., Hauffe H. C., Marchesi J., Perkins S. E. (2015a). Interactions between multiple helminths and the gut microbiota in wild rodents. PubMed DOI PMC
Kreisinger J., Čížková D., Kropáčková L., Albrecht T. (2015b). Cloacal microbiome structure in a long-distance migratory bird assessed using deep 16sRNA pyrosequencing. PubMed DOI PMC
Kreisinger J., Čížková D., Vohánka J., Piálek J. (2014). Gastrointestinal microbiota of wild and inbred individuals of two house mouse subspecies assessed using high-throughput parallel pyrosequencing. PubMed DOI
Kumar M., Babaei P., Ji B., Nielsen J. (2016). Human gut microbiota and healthy aging: recent developments and future prospective. PubMed DOI PMC
Langille M. G. I., Zaneveld J., Caporaso J. G., McDonald D., Knights D., Reyes J. A., et al. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. PubMed DOI PMC
Lewis W. B., Moore F. R., Wang S. (2016). Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico. DOI
Ley R. E., Hamady M., Lozupone C., Turnbaugh P., Ramey R. R., Bircher J. S., et al. (2008). Evolution of mammals and their gut microbes. PubMed DOI PMC
Lim M. Y., Rho M., Song Y.-M., Lee K., Sung J., Ko G. (2014). Stability of gut enterotypes in Korean monozygotic twins and their association with biomarkers and diet. PubMed DOI PMC
Liu J. R., Lai S. F., Yu B. (2007). Evaluation of an intestinal Lactobacillus reuteri strain expressing rumen fungal xylanase as a probiotic for broiler chickens fed on a wheat-based diet. PubMed DOI
Ljungh A., Wadström T. (2006). Lactic acid bacteria as probiotics. PubMed
Love M. I., Huber W., Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC
Lozupone C., Knight R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. PubMed DOI PMC
Lucas F. S., Heeb P. (2005). Environmental factors shape cloacal bacterial assemblages in great tit DOI
Mach N., Berri M., Estellé J., Levenez F., Lemonnier G., Denis C., et al. (2015). Early-life establishment of the swine gut microbiome and impact on host phenotypes. PubMed DOI
Macpherson A. J., Harris N. L. (2004). Interactions between commensal intestinal bacteria and the immune system. PubMed DOI
Maurice C. F., Cl Knowles S., Ladau J., Pollard K. S., Fenton A., Pedersen A. B., et al. (2015). Marked seasonal variation in the wild mouse gut microbiota. PubMed DOI PMC
McKnite A. M., Perez-Munoz M. E., Lu L., Williams E. G., Brewer S., Andreux P. A., et al. (2012). Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PubMed DOI PMC
McMurdie P. J., Holmes S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PubMed DOI PMC
McMurdie P. J., Holmes S. (2014). Waste not, want not: why rarefying microbiome data is inadmissible. PubMed DOI PMC
McWhorter T. J., Caviedes-Vidal E., Karasov W. H. (2009). The integration of digestion and osmoregulation in the avian gut. PubMed DOI
Møller A. P. (1994).
Morris B. E. L., Henneberger R., Huber H., Moissl-Eichinger C. (2013). Microbial syntrophy: interaction for the common good. PubMed DOI
Moya A., Ferrer M. (2016). Functional redundancy-induced stability of gut microbiota subjected to disturbance. PubMed DOI
Muegge B. D., Kuczynski J., Knights D., Clemente J. C., González A., Fontana L., et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. PubMed DOI PMC
Mulder M., Ranchor A. V., Sanderman R., Bouma J., van den Heuvel W. J. (1998). The stability of lifestyle behaviour. PubMed DOI
Org E., Mehrabian M., Parks B. W., Shipkova P., Liu X., Drake T. A., et al. (2016). Sex differences and hormonal effects on gut microbiota composition in mice. PubMed DOI PMC
Perry G. C. (2006).
Petrželková A., Michálková R., Albrechtová J., Cepák J., Honza M., Kreisinger J., et al. (2015). Brood parasitism and quasi-parasitism in the European barn swallow DOI
Plonka P. M., Grabacka M. (2006). Melanin synthesis in microorganisms–biotechnological and medical aspects. PubMed
Potrikus C. J., Breznak J. A. (1981). Gut bacteria recycle uric acid nitrogen in termites: A strategy for nutrient conservation. PubMed DOI PMC
Price M. N., Dehal P. S., Arkin A. P. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. PubMed DOI PMC
Qin J., Li R., Raes J., Arumugam M., Burgdorf K. S., Manichanh C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. PubMed DOI PMC
R Core Team (2015).
Reikvam D. H., Erofeev A., Sandvik A., Grcic V., Jahnsen F. L., Gaustad P., et al. (2011). Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PubMed DOI PMC
Riley M. A., Wertz J. E. (2002). Bacteriocins: evolution, ecology, and application. PubMed DOI
Ritchie B. W., Harrison G. J., Harrison L. R. (1994).
Ruiz F. O., Gerbaldo G., Asurmendi P., Pascual L. M., Giordano W., Barberis I. L. (2009). Antimicrobial activity, inhibition of urogenital pathogens, and synergistic interactions between lactobacillus strains. PubMed DOI
Ruiz-Rodríguez M., Lucas F. S., Heeb P., Soler J. J. (2009). Differences in intestinal microbiota between avian brood parasites and their hosts. DOI
Salminen S., Gibson G. R., McCartney A. L., Isolauri E. (2004). Influence of mode of delivery on gut microbiota composition in seven year old children. PubMed DOI PMC
Salonen A., Lahti L., Salojärvi J., Holtrop G., Korpela K., Duncan S. H., et al. (2014). Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. PubMed DOI PMC
Sanders J. G., Powell S., Kronauer D. J. C., Vasconcelos H. L., Frederickson M. E., Pierce N. E. (2014). Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. PubMed DOI
Schloss P. D., Schubert A. M., Zackular J. P., Iverson K. D., Young V. B., Petrosino J. F. (2012). Stabilization of the murine gut microbiome following weaning. PubMed DOI PMC
Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. PubMed DOI PMC
Schwager E., Bielski C., Weingart G. (2014).
Shade A., Gilbert J. A. (2015). Temporal patterns of rarity provide a more complete view of microbial diversity. PubMed DOI
Smith H. G., Montgomerie R. (1992). Male incubation in Barn Swallows: the influence of nest temperature and sexual selection. DOI
Smith M. I., Yatsunenko T., Manary M. J., Trehan I., Mkakosya R., Cheng J., et al. (2013). Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. PubMed DOI PMC
Sommer F., Ståhlman M., Ilkayeva O., Arnemo J. M., Kindberg J., Josefsson J., et al. (2016). The gut microbiota modulates energy metabolism in the hibernating brown bear PubMed DOI
Sommer S. (2005). The importance of immune gene variability (MHC) in evolutionary ecology and conservation. PubMed DOI PMC
Stevenson T. J., Buck C. L., Duddleston K. N. (2014). Temporal dynamics of the cecal gut microbiota of juvenile arctic ground squirrels: a strong litter effect across the first active season. PubMed DOI PMC
Storey J. D., Tibshirani R. (2003). Statistical significance for genomewide studies. PubMed DOI PMC
Sumithra T. G., Chaturvedi V. K., Susan C., Siju S. J., Rai A. K., Harish C., et al. (2013). Mycoplasmosis in wildlife: a review. DOI
Sun B., Wang X., Bernstein S., Huffman M. A., Xia D.-P., Gu Z., et al. (2016). Marked variation between winter and spring gut microbiota in free-ranging Tibetan Macaques ( PubMed DOI PMC
Tap J., Furet J.-P., Bensaada M., Philippe C., Roth H., Rabot S., et al. (2015). Gut microbiota richness promotes its stability upon increased dietary fibre intake in healthy adults. PubMed DOI
Thong-On A., Suzuki K., Noda S., Inoue J., Kajiwara S., Ohkuma M. (2012). Isolation and characterization of anaerobic bacteria for symbiotic recycling of uric acid nitrogen in the gut of various termites. PubMed DOI PMC
Turner A. K. (1980).
Waite D. W., Eason D. K., Taylor M. W. (2014). Influence of hand rearing and bird age on the fecal microbiota of the critically endangered kakapo. PubMed DOI PMC
Wang J., Kalyan S., Steck N., Turner L. M., Harr B., Künzel S., et al. (2015). Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome. PubMed DOI PMC
Wang J., Linnenbrink M., Künzel S., Fernandes R., Nadeau M.-J., Rosenstiel P., et al. (2014). Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. PubMed DOI PMC
Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. PubMed DOI PMC
White J., Mirleau P., Danchin E., Mulard H., Hatch S. A., Heeb P., et al. (2010). Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. PubMed DOI PMC
Wu H.-J., Wu E. (2012). The role of gut microbiota in immune homeostasis and autoimmunity. PubMed DOI PMC
Xenoulis P. G., Gray P. L., Brightsmith D., Palculict B., Hoppes S., Steiner J. M., et al. (2010). Molecular characterization of the cloacal microbiota of wild and captive parrots. PubMed DOI
Yoshimoto S., Loo T. M., Atarashi K., Kanda H., Sato S., Oyadomari S., et al. (2013). Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. PubMed DOI
Yuan M. L., Dean S. H., Longo A. V., Rothermel B. B., Tuberville T. D., Zamudio K. R. (2015). Kinship, inbreeding and fine-scale spatial structure influence gut microbiota in a hindgut-fermenting tortoise. PubMed DOI
Yurkovetskiy L., Burrows M., Khan A. A., Graham L., Volchkov P., Becker L., et al. (2013). Gender bias in autoimmunity is influenced by microbiota. PubMed DOI PMC
Zhang J., Kobert K., Flouri T., Stamatakis A. (2014). PEAR: a fast and accurate Illumina Paired-End reAd mergeR. PubMed DOI PMC
Zilber-Rosenberg I., Rosenberg E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. PubMed DOI
Nearly (?) sterile avian egg in a passerine bird
Gut microbiota variation between climatic zones and due to migration strategy in passerine birds
Variation in diet composition and its relation to gut microbiota in a passerine bird
Seasonal and Sexual Differences in the Microbiota of the Hoopoe Uropygial Secretion