Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs
Abstract The gut microbiome plays important roles in the maintenance of health and pathogenesis of diseases in the growing host. In order to fully comprehend the interplay of the gut microbiome and host, a foundational understanding of longitudinal microbiome, including bacteria and fungi, developme...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2022-09-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-19093-9 |
| _version_ | 1811273563256127488 |
|---|---|
| author | Brandi Feehan Qinghong Ran Victoria Dorman Kourtney Rumback Sophia Pogranichniy Kaitlyn Ward Robert Goodband Megan C. Niederwerder Katie Lynn Summers Sonny T. M. Lee |
| author_facet | Brandi Feehan Qinghong Ran Victoria Dorman Kourtney Rumback Sophia Pogranichniy Kaitlyn Ward Robert Goodband Megan C. Niederwerder Katie Lynn Summers Sonny T. M. Lee |
| author_sort | Brandi Feehan |
| collection | DOAJ |
| description | Abstract The gut microbiome plays important roles in the maintenance of health and pathogenesis of diseases in the growing host. In order to fully comprehend the interplay of the gut microbiome and host, a foundational understanding of longitudinal microbiome, including bacteria and fungi, development is necessary. In this study, we evaluated enteric microbiome and host dynamics throughout the lifetime of commercial swine. We collected a total of 234 fecal samples from ten pigs across 31 time points in three developmental stages (5 preweaning, 15 nursery, and 11 growth adult). We then performed 16S rRNA gene amplicon sequencing for bacterial profiles and qPCR for the fungus Kazachstania slooffiae. We identified distinct bacteriome clustering according to the host developmental stage, with the preweaning stage exhibiting low bacterial diversity and high volatility amongst samples. We further identified clusters of bacteria that were considered core, increasing, decreasing or stage-associated throughout the host lifetime. Kazachstania slooffiae was absent in the preweaning stage but peaked during the nursery stage of the host. We determined that all host growth stages contained negative correlations between K. slooffiae and bacterial genera, with only the growth adult stage containing positive correlates. Our stage-associated bacteriome results suggested the neonate contained a volatile gut microbiome. Upon weaning, the microbiome became relatively established with comparatively fewer perturbations in microbiome composition. Differential analysis indicated bacteria might play distinct stage-associated roles in metabolism and pathogenesis. The lack of positive correlates and shared K. slooffiae-bacteria interactions between stages warranted future research into the interactions amongst these kingdoms for host health. This research is foundational for understanding how bacteria and fungi develop singularly, as well as within a complex ecosystem in the host’s gut environment. |
| first_indexed | 2024-04-12T23:01:43Z |
| format | Article |
| id | doaj.art-d50653494ff943cdb1f53dbc9c3511d8 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-12T23:01:43Z |
| publishDate | 2022-09-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-d50653494ff943cdb1f53dbc9c3511d82022-12-22T03:13:02ZengNature PortfolioScientific Reports2045-23222022-09-0112111210.1038/s41598-022-19093-9Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigsBrandi Feehan0Qinghong Ran1Victoria Dorman2Kourtney Rumback3Sophia Pogranichniy4Kaitlyn Ward5Robert Goodband6Megan C. Niederwerder7Katie Lynn Summers8Sonny T. M. Lee9Division of Biology, College of Arts and Sciences, Kansas State UniversityDivision of Biology, College of Arts and Sciences, Kansas State UniversityDivision of Biology, College of Arts and Sciences, Kansas State UniversityDivision of Biology, College of Arts and Sciences, Kansas State UniversityDivision of Biology, College of Arts and Sciences, Kansas State UniversityDivision of Biology, College of Arts and Sciences, Kansas State UniversityDepartment of Animal Sciences and Industry, College of Agriculture, Kansas State UniversityDepartment of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State UniversityAnimal Biosciences and Biotechnology Laboratory, Beltsville Agricultural Research Center, Agricultural Research Center, United States Department of AgricultureDivision of Biology, College of Arts and Sciences, Kansas State UniversityAbstract The gut microbiome plays important roles in the maintenance of health and pathogenesis of diseases in the growing host. In order to fully comprehend the interplay of the gut microbiome and host, a foundational understanding of longitudinal microbiome, including bacteria and fungi, development is necessary. In this study, we evaluated enteric microbiome and host dynamics throughout the lifetime of commercial swine. We collected a total of 234 fecal samples from ten pigs across 31 time points in three developmental stages (5 preweaning, 15 nursery, and 11 growth adult). We then performed 16S rRNA gene amplicon sequencing for bacterial profiles and qPCR for the fungus Kazachstania slooffiae. We identified distinct bacteriome clustering according to the host developmental stage, with the preweaning stage exhibiting low bacterial diversity and high volatility amongst samples. We further identified clusters of bacteria that were considered core, increasing, decreasing or stage-associated throughout the host lifetime. Kazachstania slooffiae was absent in the preweaning stage but peaked during the nursery stage of the host. We determined that all host growth stages contained negative correlations between K. slooffiae and bacterial genera, with only the growth adult stage containing positive correlates. Our stage-associated bacteriome results suggested the neonate contained a volatile gut microbiome. Upon weaning, the microbiome became relatively established with comparatively fewer perturbations in microbiome composition. Differential analysis indicated bacteria might play distinct stage-associated roles in metabolism and pathogenesis. The lack of positive correlates and shared K. slooffiae-bacteria interactions between stages warranted future research into the interactions amongst these kingdoms for host health. This research is foundational for understanding how bacteria and fungi develop singularly, as well as within a complex ecosystem in the host’s gut environment.https://doi.org/10.1038/s41598-022-19093-9 |
| spellingShingle | Brandi Feehan Qinghong Ran Victoria Dorman Kourtney Rumback Sophia Pogranichniy Kaitlyn Ward Robert Goodband Megan C. Niederwerder Katie Lynn Summers Sonny T. M. Lee Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs Scientific Reports |
| title | Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs |
| title_full | Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs |
| title_fullStr | Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs |
| title_full_unstemmed | Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs |
| title_short | Stability and volatility shape the gut bacteriome and Kazachstania slooffiae dynamics in preweaning, nursery and adult pigs |
| title_sort | stability and volatility shape the gut bacteriome and kazachstania slooffiae dynamics in preweaning nursery and adult pigs |
| url | https://doi.org/10.1038/s41598-022-19093-9 |
| work_keys_str_mv | AT brandifeehan stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT qinghongran stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT victoriadorman stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT kourtneyrumback stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT sophiapogranichniy stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT kaitlynward stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT robertgoodband stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT megancniederwerder stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT katielynnsummers stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs AT sonnytmlee stabilityandvolatilityshapethegutbacteriomeandkazachstaniaslooffiaedynamicsinpreweaningnurseryandadultpigs |