skip to main content

Title: Gut microbiomes of sympatric Amazonian wood‐eating catfishes (Loricariidae) reflect host identity and little role in wood digestion
Neotropical wood‐eating catfishes (family Loricariidae) can occur in diverse assemblages with multiple genera and species feeding on the same woody detritus. As such, they present an intriguing system in which to examine the influence of host species identity on the vertebrate gut microbiome as well as to determine the potential role of gut bacteria in wood digestion. We characterized the gut microbiome of two co‐occurring catfish genera and four species: Panaqolus albomaculatus , Panaqolus gnomus , Panaqolus nocturnus, and Panaque bathyphilus , as well as that of submerged wood on which they feed. The gut bacterial community did not significantly vary across three gut regions (proximal, mid, distal) for any catfish species, although interspecific variation in the gut microbiome was significant, with magnitude of interspecific difference generally reflecting host phylogenetic proximity. Further, the gut microbiome of each species was significantly different to that present on the submerged wood. Inferring the genomic potential of the gut microbiome revealed that the majority of wood digesting pathways were at best equivalent to and more often depleted or nonexistent within the catfish gut compared to the submerged wood, suggesting a minimal role for the gut microbiome in wood digestion. Rather, these fishes are more more » likely reliant on fiber degradation performed by microbes in the environment, with their gut microbiome determined more by host identity and phylogenetic history. « less
; ; ;
Award ID(s):
Publication Date:
Journal Name:
Ecology and Evolution
Sponsoring Org:
National Science Foundation
More Like this
  1. Hird, Sarah M. (Ed.)
    The gut microbiome provides vital functions for mammalian hosts, yet research on its variability and function across adult life spans and multiple generations is limited in large mammalian carnivores. Here, we used 16S rRNA gene and metagenomic high-throughput sequencing to profile the bacterial taxonomic composition, genomic diversity, and metabolic function of fecal samples collected from 12 wild spotted hyenas ( Crocuta crocuta ) residing in the Masai Mara National Reserve, Kenya, over a 23-year period spanning three generations. The metagenomic data came from four of these hyenas and spanned two 2-year periods. With these data, we determined the extent to which host factors predicted variation in the gut microbiome and identified the core microbes present in the guts of hyenas. We also investigated novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition varied temporally, but despite this, a core set of 14 bacterial genera were identified. The strongest predictors of the microbiome were host identity and age, suggesting that hyenas possess individualized microbiomes and that these may change with age during adulthood. The gut microbiome functional profiles of the four adult hyenas were also individual specificmore »and were associated with prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyenas’ guts; some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species-level matches to genomes in existing reference databases. IMPORTANCE There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host’s life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts. We also recovered 149 high-quality MAGs from the hyena gut, greatly expanding the microbial genome repertoire known for hyenas, carnivores, and wild mammals in general. Some MAGs came from genera abundant in the gastrointestinal tracts of canid species and other carnivores, but over 80% of MAGs were novel and from species not previously represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of nonmodel wild hosts, using multiple sequencing methods and computational approaches and at distinct scales of analysis.« less
  2. Shipworms are ecologically and economically important mollusks that feed on woody plant material (lignocellulosic biomass) in marine environments. Digestion occurs in a specialized cecum, reported to be virtually sterile and lacking resident gut microbiota. Wood-degrading CAZymes are produced both endogenously and by gill endosymbiotic bacteria, with extracellular enzymes from the latter being transported to the gut. Previous research has predominantly focused on how these animals process the cellulose component of woody plant material, neglecting the breakdown of lignin – a tough, aromatic polymer which blocks access to the holocellulose components of wood. Enzymatic or non-enzymatic modification and depolymerization of lignin has been shown to be required in other wood-degrading biological systems as a precursor to cellulose deconstruction. We investigated the genomes of five shipworm gill bacterial symbionts obtained from the Joint Genome Institute Integrated Microbial Genomes and Microbiomes Expert Review for the production of lignin-modifying enzymes, or ligninases. The genomes were searched for putative ligninases using the Joint Genome Institute’s Function Profile tool and blastp analyses. The resulting proteins were then modeled using SWISS-MODEL. Although each bacterial genome possessed at least four predicted ligninases, the percent identities and protein models were of low quality and were unreliable. Prior research demonstratesmore »limited endogenous ability of shipworms to modify lignin at the chemical/molecular level. Similarly, our results reveal that shipworm bacterial gill-symbiont enzymes are unlikely to play a role in lignin modification during lignocellulose digestion in the shipworm gut. This suggests that our understanding of how these keystone organisms digest and process lignocellulose is incomplete, and further research into non-enzymatic and/or other unknown mechanisms for lignin modification is required.« less
  3. In spite of their indispensable role in host nutrition, the anaerobic gut fungal (AGF) component of the herbivorous gut microbiome remains poorly characterized. To examine global patterns and determinants of AGF diversity, we generated and analyzed an amplicon dataset from 661 fecal samples from 34 animal species, 9 families, and 6 continents. We identified 56 novel genera, greatly expanding AGF diversity beyond current estimates. Both stochastic (homogenizing dispersal and drift) and deterministic (homogenizing selection) processes played an integral role in shaping AGF communities, with a higher level of stochasticity observed in foregut fermenters. Community structure analysis revealed a distinct pattern of phylosymbiosis, where host-associated (animal species, family, and gut type), rather than ecological (domestication status and biogeography) factors predominantly shaped the community. Hindgut fermenters exhibited stronger and more specific fungal-host associations, compared to broader mostly non-host specific associations in foregut fermenters. Transcriptomics-enabled phylogenomic and molecular clock analyses of 52 strains from 14 genera indicated that most genera with preferences for hindgut hosts evolved earlier (44-58 Mya), while those with preferences for foregut hosts evolved more recently (22-32 Mya). This pattern is in agreement with the sole dependence of herbivores on hindgut fermentation past the Cretaceous-Paleogene (K-Pg) extinction event through themore »Paleocene and Eocene, and the later rapid evolution of animals employing foregut fermentation strategy during the early Miocene. Only a few AGF genera deviated from this pattern of co-evolutionary phylosymbiosis, by exhibiting preferences suggestive of post-evolutionary environmental filtering. Our results greatly expand the documented scope of AGF diversity and provide an ecologically and evolutionary-grounded model to explain the observed patterns of AGF diversity in extant animal hosts.« less
  4. Abstract Background

    Empirical field studies allow us to view how ecological and environmental processes shape the biodiversity of our planet, but collecting samples in situ creates inherent challenges. The majority of empirical vertebrate gut microbiome research compares multiple host species against abiotic and biotic factors, increasing the potential for confounding environmental variables. To minimize these confounding factors, we focus on a single species of passerine bird found throughout the geologically complex island of Sulawesi, Indonesia. We assessed the effects of two environmental factors, geographic Areas of Endemism (AOEs) and elevation, as well as host sex on the gut microbiota assemblages of the Sulawesi Babbler,Pellorneum celebense,from three different mountains across the island. Using cloacal swabs, high-throughput-amplicon sequencing, and multiple statistical models, we identified the core microbiome and determined the signal of these three factors on microbial composition.


    The five most prevalent bacterial phyla within the gut microbiome ofP. celebensewereProteobacteria(32.6%),Actinobacteria(25.2%),Firmicutes(22.1%),Bacteroidetes(8.7%), andPlantomycetes(2.6%). These results are similar to those identified in prior studies of passeriform microbiomes. Overall, microbiota diversity decreased as elevation increased, irrespective of sex or AOE. A single ASV ofClostridiumwas enriched in higher elevation samples, while lower elevation samples were enriched with the generaPerlucidibaca(FamilyMoraxellaceae),Lachnoclostridium(FamilyLachnospiraceae), and an unidentified species in the FamilyPseudonocardiaceae.


    While themore »core microbiota families recovered here are consistent with other passerine studies, the decreases in diversity as elevation increases has only been seen in non-avian hosts. Additionally, the increased abundance ofClostridiumat high elevations suggests a potential microbial response to lower oxygen levels. This study emphasizes the importance of incorporating multiple statistical models and abiotic factors such as elevation in empirical microbiome research, and is the first to describe an avian gut microbiome from the island of Sulawesi.

    « less
  5. Loranthaceae are parasitic plants in about 76 genera that are predominantly found in subtropical and temperate regions of the Southern Hemisphere as branch parasites. Australia is an area of high diversity with about 11 genera and 65 species, most of which are endemic. Loranthaceae branch parasites are also morphologically diverse having both radial and zygomorphic flowers that are typically bird pollinated and each of the four basic haustorial types. Haustorial types include epicortical roots (ERs) that grow along the host branch surface and at intervals form secondary attachments to their host, clasping unions where parasite tissue enlarges partially encircling the host branch, wood roses where host tissue proliferates forming a placenta where the parasite is attached, and bark strands that spread within the outer tissues of the host branch. We hypothesized that those haustoria where parasitic tissue proliferated, such as ERs and clasping unions, would occupy more mesic environments. To test this hypothesis and investigate other relationships among ecological parameters and haustorial form we used 17,753 sets of occurrence and ecological data from the Atlas of Living Australia (ALA) online repository for 42 species of Loranthaceae. We analyzed haustorial forms through comparative studies of haustoria housed at the UC Herbarium,more »relevant literature, and collections in public repositories. Biogeographical and environmental data were analyzed using mapping and statistical methods in the R environment. Our preliminary research suggests that bark strands are found in climatic regions across Australia, including deserts, while both epicortical roots (ERs) and clasping unions are mostly restricted to mesic coastlines of eastern Australia (21 of 22 species with ERs occur only along eastern coastlines of Australia or in the Cape York Peninsula). Wood roses are less common in Australia with few data points. Haustoria are sometimes complex, especially clasping unions where bark strands are occasionally also produced. An interesting finding was that Amyema sanguinea has a wide distribution in arid as well as mesic climates even though it has ERs. This species has unusually robust ERs that might contribute to its wider ecological niche. Evolution of haustoria in Australia is discussed based on phylogenetic hypotheses of Loranthaceae genera.« less