Limits...
Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae).

Estes AM, Hearn DJ, Snell-Rood EC, Feindler M, Feeser K, Abebe T, Dunning Hotopp JC, Moczek AP - PLoS ONE (2013)

Bottom Line: Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung.Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus.The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber.

View Article: PubMed Central - PubMed

Affiliation: Towson University, Department of Biological Sciences, Baltimore, Maryland, United States of America ; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America.

ABSTRACT
Insects feeding on plant sap, blood, and other nutritionally incomplete diets are typically associated with mutualistic bacteria that supplement missing nutrients. Herbivorous mammal dung contains more than 86% cellulose and lacks amino acids essential for insect development and reproduction. Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung. These associations suggest that dung beetles may benefit from mutualistic bacteria that provide nutrients missing from dung. The nesting behaviors of the female parent and the feeding behaviors of the larvae suggest that a microbiome could be vertically transmitted from the parental female to her offspring through the brood ball. Using sterile rearing and a combination of molecular and culture-based techniques, we examine transmission of the microbiome in the bull-headed dung beetle, Onthophagus taurus. Beetles were reared on autoclaved dung and the microbiome was characterized across development. A ~1425 bp region of the 16S rRNA identified Pseudomonadaceae, Enterobacteriaceae, and Comamonadaceae as the most common bacterial families across all life stages and populations, including cultured isolates from the 3(rd) instar digestive system. Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus. Scanning electron micrographs of brood balls constructed from sterile dung reveals secretions and microbes only in the chamber the female prepares for the egg. The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber. The transmission of the dung beetle microbiome highlights the maintenance and likely importance of this newly-characterized bacterial community.

Show MeSH

Related in: MedlinePlus

Abundance of lowest common ancestors across all microbiome samples.Bacterial OTUs identified in Qiime are arranged in a bulls-eye configuration with the most commonly occurring group in the yellow center, those occurring in two or more individuals in the blue circle, and those genera occurring only one time in the outermost rim. The lowest common ancestor Qiime classification is given and may be at the genus, family, or class level and as such may overlap. Enterobacter was found in offspring of all parental females and in 68% of the individuals. Samples denoted with a star are those OTUs that were found using both culture-dependent and -independent techniques.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3815100&req=5

pone-0079061-g005: Abundance of lowest common ancestors across all microbiome samples.Bacterial OTUs identified in Qiime are arranged in a bulls-eye configuration with the most commonly occurring group in the yellow center, those occurring in two or more individuals in the blue circle, and those genera occurring only one time in the outermost rim. The lowest common ancestor Qiime classification is given and may be at the genus, family, or class level and as such may overlap. Enterobacter was found in offspring of all parental females and in 68% of the individuals. Samples denoted with a star are those OTUs that were found using both culture-dependent and -independent techniques.

Mentions: OTUs were assigned using the CloVR pipeline with a 95% threshold as described in the methods for the 275 16S rRNA sequences obtained. Predicted chimeric sequences (n=4) as well as sequences shorter than 470 bp (n=6) were discarded. From the 265 remaining sequences, 71 OTUs were identified across 19 individuals. Of those 71 OTUs, 49 OTUs were classified to the family level, 4 to the phylum level, and 4 could not be classified further than “root” (Figures 3, 4, and 5). The most abundant genus found across all samples was Enterobacter (Figures 3, 4, and 5).


Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae).

Estes AM, Hearn DJ, Snell-Rood EC, Feindler M, Feeser K, Abebe T, Dunning Hotopp JC, Moczek AP - PLoS ONE (2013)

Abundance of lowest common ancestors across all microbiome samples.Bacterial OTUs identified in Qiime are arranged in a bulls-eye configuration with the most commonly occurring group in the yellow center, those occurring in two or more individuals in the blue circle, and those genera occurring only one time in the outermost rim. The lowest common ancestor Qiime classification is given and may be at the genus, family, or class level and as such may overlap. Enterobacter was found in offspring of all parental females and in 68% of the individuals. Samples denoted with a star are those OTUs that were found using both culture-dependent and -independent techniques.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3815100&req=5

pone-0079061-g005: Abundance of lowest common ancestors across all microbiome samples.Bacterial OTUs identified in Qiime are arranged in a bulls-eye configuration with the most commonly occurring group in the yellow center, those occurring in two or more individuals in the blue circle, and those genera occurring only one time in the outermost rim. The lowest common ancestor Qiime classification is given and may be at the genus, family, or class level and as such may overlap. Enterobacter was found in offspring of all parental females and in 68% of the individuals. Samples denoted with a star are those OTUs that were found using both culture-dependent and -independent techniques.
Mentions: OTUs were assigned using the CloVR pipeline with a 95% threshold as described in the methods for the 275 16S rRNA sequences obtained. Predicted chimeric sequences (n=4) as well as sequences shorter than 470 bp (n=6) were discarded. From the 265 remaining sequences, 71 OTUs were identified across 19 individuals. Of those 71 OTUs, 49 OTUs were classified to the family level, 4 to the phylum level, and 4 could not be classified further than “root” (Figures 3, 4, and 5). The most abundant genus found across all samples was Enterobacter (Figures 3, 4, and 5).

Bottom Line: Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung.Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus.The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber.

View Article: PubMed Central - PubMed

Affiliation: Towson University, Department of Biological Sciences, Baltimore, Maryland, United States of America ; Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America.

ABSTRACT
Insects feeding on plant sap, blood, and other nutritionally incomplete diets are typically associated with mutualistic bacteria that supplement missing nutrients. Herbivorous mammal dung contains more than 86% cellulose and lacks amino acids essential for insect development and reproduction. Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung. These associations suggest that dung beetles may benefit from mutualistic bacteria that provide nutrients missing from dung. The nesting behaviors of the female parent and the feeding behaviors of the larvae suggest that a microbiome could be vertically transmitted from the parental female to her offspring through the brood ball. Using sterile rearing and a combination of molecular and culture-based techniques, we examine transmission of the microbiome in the bull-headed dung beetle, Onthophagus taurus. Beetles were reared on autoclaved dung and the microbiome was characterized across development. A ~1425 bp region of the 16S rRNA identified Pseudomonadaceae, Enterobacteriaceae, and Comamonadaceae as the most common bacterial families across all life stages and populations, including cultured isolates from the 3(rd) instar digestive system. Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus. Scanning electron micrographs of brood balls constructed from sterile dung reveals secretions and microbes only in the chamber the female prepares for the egg. The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber. The transmission of the dung beetle microbiome highlights the maintenance and likely importance of this newly-characterized bacterial community.

Show MeSH
Related in: MedlinePlus