An official website of the United States government
Abstract Maternal transmission of microbes occurs across the animal kingdom and is vital for offspring development and long-term health. The mechanisms of this transfer are most well-studied in humans and other mammals but are less well-understood in egg-laying animals, especially those with no parental care. Here, we investigate the transfer of maternal microbes in the oviparous phrynosomatid lizard, Sceloporus virgatus. We compared the microbiota of three maternal tissues—oviduct, cloaca, and intestine—to three offspring sample types: egg contents and eggshells on the day of oviposition, and hatchling intestinal tissue on the day of hatching. We found that maternal identity is an important factor in hatchling microbiome composition, indicating that maternal transmission is occurring. The maternal cloacal and oviductal communities contribute to offspring microbiota in all three sample types, with minimal microbes sourced from maternal intestines. This indicates that the maternal reproductive microbiome is more important for microbial inheritance than the gut microbiome, and the tissue-level variation of the adult S. virgatus microbiota must develop as the hatchling matures. Despite differences between adult and hatchling communities, offspring microbiota were primarily members of the Enterobacteriaceae and Yersiniaceae families (Phylum Proteobacteria), consistent with this and past studies of adult S. virgatus microbiomes.
more »
« less
Recovered microbiome of an oviparous lizard differs across gut and reproductive tissues, cloacal swabs, and faeces
Abstract Microbial diversity and community function are related, and can be highly specialized in different gut regions. The cloacal microbiome ofSceloporus virgatusfemales provides antifungal protection to eggshells, a specialized function that suggests a specialized microbiome. Here, we describe the cloacal, intestinal, and oviductal microbiome fromS.virgatusgravid females, adding to growing evidence of microbiome localization in reptiles and other taxa. We further assessed whether common methods for sampling gastrointestinal (GI) microbes – cloacal swabs and faeces – provide accurate representations of these microbial communities. We found that different regions of the gut had unique microbial communities. The cloacal microbiome showed extreme specialization averaging 99% Proteobacteria (Phylum) and 83%Enterobacteriacaea(Family).Enterobacteriacaeadecreased up the GI and reproductive tracts. Cloacal swabs recovered communities similar to that of lower intestine and cloacal tissues. In contrast, faecal samples had much higher diversity and a distinct composition (common Phyla: 62% Firmicutes, 18% Bacteroidetes, 10% Proteobacteria; common families: 39%Lachnospiraceae, 11%Ruminococcaceae, 11%Bacteroidaceae) relative to all gut regions. The common families in faecal samples made up <1% of cloacal tissue samples, increasing to 43% at the upper intestine. Similarly, the common families in gut tissue (EnterobacteriaceaeandHelicobacteraceae) made up <1% of the faecal microbiome. Further, we found that cloacal swabs taken shortly after defaecation may be contaminated with faecal matter. Our results serve as a caution against using faeces as a proxy for GI microbes, and may help explain high between‐sample variation seen in some studies using cloacal swabs.
more »
« less
- Award ID(s):
- 1755408
- PAR ID:
- 10367926
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology Resources
- Volume:
- 22
- Issue:
- 5
- ISSN:
- 1755-098X
- Page Range / eLocation ID:
- p. 1693-1705
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Investigating animal gut microbiomes can lead to a better understanding of their foraging preferences and their overall health. In this study, the fecal and cloacal microbiomes of 4 cold-stunned, frozen loggerhead Caretta caretta, 9 Kemp’s ridley Lepidochelys kempi , and 5 green sea turtles Chelonia mydas that stranded on beaches in Massachusetts, USA, were surveyed. Cloacal swabs and in situ fecal samples were collected from each turtle. From the extracted DNA, the hypervariable V1-V3 regions of the 16S rRNA gene were amplified with PCR, then sequenced using next generation Illumina MiSeq technology. Fecal and cloacal microbiomes were primarily composed of the phyla Proteobacteria , Bacteroidetes , and Firmicutes . Microbial communities varied significantly based on location of the gut sampled. Cloacal samples were largely dominated by Proteobacteria , while fecal samples appeared to have a greater distribution of taxa and higher alpha diversity. Green turtles had a higher abundance of Firmicutes and Bacteroidetes than Kemp’s ridley and loggerhead turtles, but a lower abundance of Proteobacteria . The information gained from this study contributes to knowledge of cold-stunned sea turtle gut microbiomes and may eventually be applied to rehabilitation efforts.more » « less
-
Abstract Long-term studies of animal microbiomes under natural conditions are valuable for understanding the effects of host demographics and environmental factors on host-associated microbial communities, and how those effects interact and shift over time. We examined how the cloacal microbiome of wild Sceloporus virgatus (the striped plateau lizard) varies under natural conditions in a multi-year study. Cloacal swabs were collected from wild-caught lizards across their entire active season and over three years in southeastern Arizona, USA. Analyses of 16S rRNA data generated on the Illumina platform revealed that cloacal microbiomes of S. virgatus vary as a function of season, sex, body size, and reproductive state, and do so independently of one another. Briefly, microbial diversity was lowest in both sexes during the reproductive season, was higher in females than in males, and was lowest in females when they were vitellogenic, and microbiome composition varied across seasons, sexes, and sizes. The pattern of decreased diversity during reproductive periods with increased sociality is surprising, as studies in other systems often suggest that microbial diversity generally increases with sociality. The cloacal microbiome was not affected significantly by hibernation and was relatively stable from year to year. This study highlights the importance of long term, wide-scale microbiome studies for capturing accurate perspectives on microbiome diversity and composition in animals. It also serves as a warning for comparisons of microbiomes across species, as each may be under a different suite of selective pressures or exhibit short-term variation from external or innate factors, which may differ in a species-specific manner.more » « less
-
Comparing the diversity of gut microbiota between and within social insect colonies can illustrate interactions between bacterial community composition and host behaviour. In many eusocial insect species, different workers exhibit different task behaviours. Evidence of compositional differences between core microbiota in different worker types could suggest a microbial association with the division of labour among workers. Here, we present the core microbiota ofAphaenogaster piceaant workers with different task behaviours. The genusAphaenogasteris abundant worldwide, yet the associated microbiota of this group is unstudied. Bacterial communities fromAphaenogaster piceagut samples in this study consist of 19 phyla, dominated by Proteobacteria, Cyanobacteria and Firmicutes. Analysis of 16S rRNA gene sequences reveals distinct similarity clustering ofAphaenogaster piceagut bacterial communities in workers that have more interactions with the refuse piles. Though gut bacterial communities of nurse and foraging ants are similar in overall composition and structure, the worker groups differ in relative abundances of dominant taxa. Gut bacterial communities from ants that have more interactions with refuse piles are dominated by amplicon sequence variants associated with Entomoplasmataceae. Interaction with faecal matter via refuse piles seems to have the greatest impact on microbial taxa distribution, and this effect appears to be independent of worker type. This is the first report surveying the gut microbiome community composition ofAphaenogasterants.more » « less
-
The gut is a well-established route of infection and target for viral damage by SARSCoV-2. This is supported by the clinical observation that about half of COVID-19 patients exhibit gastrointestinal (GI) symptoms. We asked whether the analysis of plasma could provide insight into gut barrier dysfunction in patients with COVID-19 infection. Plasma samples of COVID-19 patients (n=30) and healthy control (n=16) were collected during hospitalization. Plasma microbiome was analyzed using 16S rRNA sequencing, metatranscriptomic analysis, and gut permeability markers including FABP-2, PGN and LPS in both patient cohorts. Almost 65% (9 out 14) COVID-19 patients showed abnormal presence of gut microbes in their bloodstream. Plasma samples contained predominately Proteobacteria, Firmicutes, and Actinobacteria. The abundance of gram-negative bacteria (Acinetobacter, Nitrospirillum, Cupriavidus, Pseudomonas, Aquabacterium, Burkholderia, Caballeronia, Parabhurkholderia, Bravibacterium, and Sphingomonas) was higher than the gram-positive bacteria (Staphylococcus and Lactobacillus) in COVID-19 subjects. The levels of plasma gut permeability markers FABP2 (1282±199.6 vs 838.1±91.33; p=0.0757), PGN (34.64±3.178 vs 17.53±2.12; p<0.0001), and LPS (405.5±48.37 vs 249.6±17.06; p=0.0049) were higher in COVID-19 patients compared to healthy subjects. These findings support that the intestine may represent a source for bacteremia and may contribute to worsening COVID-19 outcomes. Therapies targeting the gut and prevention of gut barrier defects may represent a strategy to improve outcomes in COVID19 patients.more » « less
