Bacterial Community in the Crop of the Hoatzin, a Neotropical Folivorous Flying Bird

ABSTRACT The hoatzin is unique among known avian species because of the fermentative function of its enlarged crop. A small-bodied flying foregut fermenter is a paradox, and this bird provides an interesting model to examine how diet selection and the gut microbiota contribute to maximizing digestive efficiency. Therefore, we characterized the bacterial population in the crop of six adult hoatzins captured from the wild. A total of 1,235 16S rRNA gene sequences were grouped into 580 phylotypes (67% of the pooled species richness sampled, based on Good's coverage estimator, with CACE and Chao1 estimates of 1,709 and 1,795 species-level [99% identity] operational taxonomic units, respectively). Members of 9 of the ∼75 known phyla in Bacteria were identified in this gut habitat; the Firmicutes were dominant (67% of sequences, belonging to the classes Clostridia, Mollicutes, and Bacilli), followed by the Bacteroidetes (30%, mostly in the order Bacteroidales), Proteobacteria (1.8%), and Lentisphaerae, Verrucomicrobia, TM7, Spirochaetes, Actinobacteria, and Aminanaerobia (all <0.1%). The novelty in this ecosystem is great; 94% of the phylotypes were unclassified at the “species” level and thus likely include novel cellulolytic lineages.

[1]  Thomas Huber,et al.  Bellerophon: a program to detect chimeric sequences in multiple sequence alignments , 2004, Bioinform..

[2]  A. Craig,et al.  Molecular Characterization of Sheep Ruminal Enrichments that Detoxify Pyrrolizidine Alkaloids by Denaturing Gradient Gel Electrophoresis and Cloning , 2007, Microbial Ecology.

[3]  Alejandro Grajal,et al.  PASSAGE RATES OF DIGESTA MARKERS IN THE GUT OF THE HOATZIN, A FOLIVOROUS BIRD WITH FOREGUT FERMENTATION' , 1995 .

[4]  E. C. Pielou The measurement of diversity in different types of biological collections , 1966 .

[5]  C. Stevens,et al.  Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. , 1998, Physiological reviews.

[6]  C. E. SHANNON,et al.  A mathematical theory of communication , 1948, MOCO.

[7]  S. O’Brien,et al.  Placental mammal diversification and the Cretaceous–Tertiary boundary , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Joerger,et al.  16S rRNA-Based Analysis of Microbiota from the Cecum of Broiler Chickens , 2002, Applied and Environmental Microbiology.

[9]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[10]  M. Dominguez-Bello,et al.  Microbial Digestive Symbionts of the Crop of the Hoatzin (Opisthocomus hoazin): An Avian Foregut Fermenter , 1993, Physiological Zoology.

[11]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[12]  J. Kornegay Molecular genetics and evolution of stomach and nonstomach lysozymes in the hoatzin , 1996, Journal of Molecular Evolution.

[13]  K. Konstantinidis,et al.  Genomic insights that advance the species definition for prokaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Bayles,et al.  Comparison of the Cecal Microbiota of Domestic and Wild Turkeys , 2008, Microbial Ecology.

[15]  K. Schleifer,et al.  ARB: a software environment for sequence data. , 2004, Nucleic acids research.

[16]  J. Cracraft A NEW FAMILY OF HOATZIN-LIKE BIRDS (ORDER OPISTHOCOMIFORMES) FROM THE EOCENE OF SOUTH AMERICA , 2008 .

[17]  Zhongtang Yu,et al.  Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing. , 2005, Environmental microbiology.

[18]  R. E. Hungate,et al.  The Rumen and Its Microbes , 2013 .

[19]  F. Bäckhed,et al.  Obesity alters gut microbial ecology. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Philip Hugenholtz,et al.  NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes , 2006, Nucleic Acids Res..

[21]  W. D. de Jong,et al.  Phylogenetic relationships of the hoatzin, an enigmatic South American bird. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[22]  R. Jones,et al.  Comparison of the digestive ability of crop fluid from the folivorous Hoatzin (Opisthocomus hoazin) and cow rumen fluid with seven tropical forages , 2000 .

[23]  Martin J Blaser,et al.  Bacterial biota in the human distal esophagus , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Alejandro Grajal Digestive efficiency of the Hoatzin, Opisthocomus hoazin: a folivorous bird with foregut fermentation , 2008 .

[25]  Alejandro Grajal STRUCTURE AND FUNCTION OF THE DIGESTIVE TRACT OF THE HOATZIN (OPISTHOCOMUS HOAZIN): A FOLIVOROUS BIRD WITH FOREGUT FERMENTATION , 1995 .

[26]  J. Handelsman,et al.  Introducing DOTUR, a Computer Program for Defining Operational Taxonomic Units and Estimating Species Richness , 2005, Applied and Environmental Microbiology.

[27]  R. Mackie,et al.  Novel Rumen Bacterial Diversity in Two Geographically Separated Sub-Species of Reindeer , 2007, Microbial Ecology.

[28]  P. V. Soest Nutritional Ecology of the Ruminant , 1994 .

[29]  M. Dominguez-Bello,et al.  Ecology of the Folivorous Hoatzin (Opisthocomus Hoazin) on the Venezuelan Plains , 1994 .

[30]  I. Good THE POPULATION FREQUENCIES OF SPECIES AND THE ESTIMATION OF POPULATION PARAMETERS , 1953 .

[31]  Montague W. Demment,et al.  A Nutritional Explanation for Body-Size Patterns of Ruminant and Nonruminant Herbivores , 1985, The American Naturalist.

[32]  K. M. Ritalahti,et al.  Dechlorination of chloroethenes is inhibited by 2-bromoethanesulfonate in the absence of methanogens , 1997, Applied and environmental microbiology.

[33]  M. Collinson,et al.  Fossil evidence of interactions between plants and plant-eating mammals. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[35]  R. Mackie,et al.  Ecology of Uncultivated Oscillospira Species in the Rumen of Cattle, Sheep, and Reindeer as Assessed by Microscopy and Molecular Approaches , 2003, Applied and Environmental Microbiology.

[36]  A. Chao,et al.  Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample , 2004, Environmental and Ecological Statistics.

[37]  W. Bossert,et al.  The Measurement of Diversity , 2001 .

[38]  P. Rothery,et al.  Scaling of body temperature in mammals and birds , 2007 .

[39]  A. Wilson,et al.  Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. , 1994, Molecular biology and evolution.

[40]  M. Dominguez-Bello,et al.  Bacterial detoxification of saponins in the crop of the avian foregut fermenter Opisthocomus hoazin , 2007 .

[41]  Alejandro Grajal Nutritional Ecology and Digestive Physiology of the Hoatzin Opisthocomus Hoazin a Folivorous Bird With Foregut Fermentation , 2019 .

[42]  F. T. Jung The Fire of Life , 1962 .

[43]  Xiuzhu Dong,et al.  Prokaryote diversity in the rumen of yak (Bos grunniens) and Jinnan cattle (Bos taurus) estimated by 16S rDNA homology analyses. , 2005, Anaerobe.

[44]  J. T. Sylvester,et al.  Assessment of ruminal bacterial populations and protozoal generation time in cows fed different methionine sources. , 2007, Journal of dairy science.

[45]  Y. Benno,et al.  Diet-Dependent Shifts in the Bacterial Population of the Rumen Revealed with Real-Time PCR , 2001, Applied and Environmental Microbiology.

[46]  P. Hugenholtz Exploring prokaryotic diversity in the genomic era , 2002, Genome Biology.

[47]  R. Cifelli,et al.  The "condylarths" (archaic Ungulata, Mammalia) from the early Palaeocene of Tiupampa (Bolivia): implications on the origin of the South American ungulates [X27465] Matrix Muizon and Cifelli 2000 , 2021 .

[48]  Alejandro Grajal,et al.  Foregut Fermentation in the Hoatzin, a Neotropical Leaf-Eating Bird , 1989, Science.

[49]  D. Mindell,et al.  More taxa, more characters: the hoatzin problem is still unresolved. , 2003, Molecular biology and evolution.

[50]  R. H. McBee,et al.  Rates of fermentative digestion in the howler monkey, Alouatta palliata (primates: ceboidea). , 1983, Comparative biochemistry and physiology. A, Comparative physiology.

[51]  R. E. Hungate,et al.  The anaerobic mesophilic cellulolytic bacteria. , 1950, Bacteriological reviews.

[52]  Baker,et al.  Phylogenetic relationships of the enigmatic hoatzin (Opisthocomus hoazin) resolved using mitochondrial and nuclear gene sequences , 1999, Molecular biology and evolution.

[53]  E. Purdom,et al.  Diversity of the Human Intestinal Microbial Flora , 2005, Science.