Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing

Hong, Pei‐Ying; Wheeler, Emily; Cann, Isaac; Mackie, Roderick I.

doi:10.1038/ismej.2011.33

Cited by 154 publications

(196 citation statements)

References 29 publications

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“…Further, the presence of sulfate-reducing bacteria enhances the fermentation performance of some cellulolytic bacteria in vitro (Morvan et al, 1996b). Interestingly, sulfatereducing bacteria are present in the guts of herbivorous marine iguanas (Amblyrhynchus cristatus), and are thought to explain the lack of methanogenic archaea in these animals (Hong et al, 2011). We did not investigate the presence of methanogenic archaea in our experiment.…”

Section: Discussionmentioning

confidence: 95%

Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard

Kohl

Brun

Magallanes

et al. 2016

Journal of Experimental Biology

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While herbivory is a common feeding strategy in a number of vertebrate classes, less than 4% of squamate reptiles feed primarily on plant material. It has been hypothesized that physiological or microbial limitations may constrain the evolution of herbivory in lizards. Herbivorous lizards exhibit adaptations in digestive morphology and function that allow them to better assimilate plant material. However, it is unknown whether these traits are fixed or perhaps phenotypically flexible as a result of diet. Here, we maintained a naturally omnivorous lizard, Liolaemus ruibali, on a mixed diet of 50% insects and 50% plant material, or a plant-rich diet of 90% plant material. We compared parameters of digestive performance, gut morphology and function, and gut microbial community structure between the two groups. We found that lizards fed the plant-rich diet maintained nitrogen balance and exhibited low minimum nitrogen requirements. Additionally, lizards fed the plantrich diet exhibited significantly longer small intestines and larger hindguts, demonstrating that gut morphology is phenotypically flexible. Lizards fed the plant-rich diet harbored small intestinal communities that were more diverse and enriched in Melainabacteria and Oscillospira compared with mixed diet-fed lizards. Additionally, the relative abundance of sulfate-reducing bacteria in the small intestine significantly correlated with whole-animal fiber digestibility. Thus, we suggest that physiological and microbial limitations do not sensu stricto constrain the evolution of herbivory in lizards. Rather, ecological context and fitness consequences may be more important in driving the evolution of this feeding strategy.

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Section: Discussionmentioning

confidence: 95%

Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard

Kohl

Brun

Magallanes

et al. 2016

Journal of Experimental Biology

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“…The existence of active methanogens in the gut of herbivorous lizards has been detected by methane production from fecal material of captive iguanas (Hackstein and Van Alen, 1996). Recently, Hong et al (2011) reported an investigation of hindgut microbiota in three herbivorous reptiles from the Galapagos Islands: marine iguana (Amblyrhynchus cristatus), land iguana (Conolophus sp.) and giant tortoise (Geochelone nigra).…”

Section: Reptilesmentioning

confidence: 99%

“…Whereas marine iguanas feed primarily on soft macrophytic algae growing in intertidal and subtidal zones (Shepherd and Hawkes, 2005), land iguanas and giant tortoises feed on similar species of terrestrial vegetation (Christian et al, 1984). Intriguingly, Hong et al (2011) were unable to recover archaeal sequences from marine iguanas, perhaps because of very low methanogen densities. However, archaeal sequences were successfully amplified from the feces of the other hosts sampled.…”

Section: Reptilesmentioning

confidence: 99%

Diversity of gut methanogens in herbivorous animals

St-Pierre

Wright

2013

Animal

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The digestion of plant biomass by symbiotic microbial communities in the gut of herbivore hosts also results in the production of methane, a greenhouse gas that is released into the environment where it contributes to climate change. As methane is exclusively produced by methanogenic archaea, various research groups have devoted their efforts to investigate the population structure of symbiotic methanogens in the gut of herbivores. In this review, we summarized and compared currently available results from 16S rRNA gene clone library studies, which cover a broad range of hosts from ruminant livestock species to wild ruminants, camelids, marsupials, primates, birds and reptiles. Although gut methanogens are very diverse, they tend to be limited to specific phylogenetic groups. Overall, methanogens related to species of the genus Methanobrevibacter are the most highly represented archaea in the gut of herbivores. However, under certain conditions, archaea from more phylogenetically distant groups are the most prevalent, such as methanogens belonging to either the genus Methanosphaera, the order Methanomicrobiales or the Thermoplasmatales-Affiliated Lineage C Comparisons not only highlight the strong influence of host species and diet in the determination of the population structure of symbiotic methanogens, but also reveal other complex relationships, such as wide differences between breeds, as well as unexpected similarities between unrelated species. These observations strongly support the need for high throughput sequencing and metagenomic studies to gain further insight.

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“…For many years, researchers have been trying to estimate the microbial diversity of complex environments, such as soil (9), marine systems (10), and animal gut systems (11,12). Various techniques have been developed, from culture-dependent methods to 16S rRNA genes-based methods of clone library (13,14), denaturing gradient gel electrophoresis (DGGE) (15), terminal restriction fragment length polymorphism (T-RFLP) (16), and the recently developed next-generation sequencing (17).…”

mentioning

confidence: 99%

Intragenomic Heterogeneity of 16S rRNA Genes Causes Overestimation of Prokaryotic Diversity

Sun

Jiang

et al. 2013

Appl Environ Microbiol

345

260

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bEver since Carl Woese introduced the use of 16S rRNA genes for determining the phylogenetic relationships of prokaryotes, this method has been regarded as the "gold standard" in both microbial phylogeny and ecology studies. However, intragenomic heterogeneity within 16S rRNA genes has been reported in many investigations and is believed to bias the estimation of prokaryotic diversity. In the current study, 2,013 completely sequenced genomes of bacteria and archaea were analyzed and intragenomic heterogeneity was found in 952 genomes (585 species), with 87.5% of the divergence detected being below the 1% level. In particular, some extremophiles (thermophiles and halophiles) were found to harbor highly divergent 16S rRNA genes. Overestimation caused by 16S rRNA gene intragenomic heterogeneity was evaluated at different levels using the full-length and partial 16S rRNA genes usually chosen as targets for pyrosequencing. The result indicates that, at the unique level, full-length 16S rRNA genes can produce an overestimation of as much as 123.7%, while at the 3% level, an overestimation of 12.9% for the V6 region may be introduced. Further analysis showed that intragenomic heterogeneity tends to concentrate in specific positions, with the V1 and V6 regions suffering the most intragenomic heterogeneity and the V4 and V5 regions suffering the least intragenomic heterogeneity in bacteria. This is the most up-to-date overview of the diversity of 16S rRNA genes within prokaryotic genomes. It not only provides general guidance on how much overestimation can be introduced when applying 16S rRNA gene-based methods, due to its intragenomic heterogeneity, but also recommends that, for bacteria, this overestimation be minimized using primers targeting the V4 and V5 regions. F or decades, 16S rRNA genes, which encode the small subunit of rRNA in prokaryotes, have been widely used in taxonomic assignment and phylogenetic relationship determination (1, 2). The specific properties of the 16S rRNA gene, including its ubiquitous distribution, mosaic structure (3), and relative stability (4), qualify it as an optimal choice to fulfill these applications. Although some argue that 16S rRNA genes alone may not be sufficient to identify closely related species (5, 6) and the use of monocopy genes like rpoB to perform similar studies has been proposed (7), 16S rRNA genes are undoubtedly the most widely used molecular markers in microbial ecological studies due to well-maintained databases (8) and their easy accessibility.For many years, researchers have been trying to estimate the microbial diversity of complex environments, such as soil (9), marine systems (10), and animal gut systems (11, 12). Various techniques have been developed, from culture-dependent methods to 16S rRNA genes-based methods of clone library (13, 14), denaturing gradient gel electrophoresis (DGGE) (15), terminal restriction fragment length polymorphism (T-RFLP) (16), and the recently developed next-generation sequencing (17). However, the question of how diverse an e...

show abstract

Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing

Cited by 154 publications

References 29 publications

Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard

Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard

Diversity of gut methanogens in herbivorous animals

Intragenomic Heterogeneity of 16S rRNA Genes Causes Overestimation of Prokaryotic Diversity

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