Microbiome composition and function within the Kellet’s whelk perivitelline fluid

ABSTRACTMicrobiomes have gained significant attention in ecological research, owing to their diverse interactions and essential roles within different organismal ecosystems. Microorganisms, such as bacteria, archaea, and viruses, have profound impact on host health, influencing digestion, metabolism...

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Main Authors: Benjamin N. Daniels, Jenna Nurge, Chanel De Smet, Olivia Sleeper, Crow White, Jean M. Davidson, Pat Fidopiastis
Format: Article
Language:English
Published: American Society for Microbiology 2024-03-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03514-23
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author Benjamin N. Daniels
Jenna Nurge
Chanel De Smet
Olivia Sleeper
Crow White
Jean M. Davidson
Pat Fidopiastis
author_facet Benjamin N. Daniels
Jenna Nurge
Chanel De Smet
Olivia Sleeper
Crow White
Jean M. Davidson
Pat Fidopiastis
author_sort Benjamin N. Daniels
collection DOAJ
description ABSTRACTMicrobiomes have gained significant attention in ecological research, owing to their diverse interactions and essential roles within different organismal ecosystems. Microorganisms, such as bacteria, archaea, and viruses, have profound impact on host health, influencing digestion, metabolism, immune function, tissue development, and behavior. This study investigates the microbiome diversity and function of Kellet’s whelk (Kelletia kelletii) perivitelline fluid (PVF), which sustains thousands of developing K. kelletii embryos within a polysaccharide and protein matrix. Our core microbiome analysis reveals a diverse range of bacteria, with the Roseobacter genus being the most abundant. Additionally, genes related to host-microbe interactions, symbiosis, and quorum sensing were detected, indicating a potential symbiotic relationship between the microbiome and Kellet’s whelk embryos. Furthermore, the microbiome exhibits gene expression related to antibiotic biosynthesis, suggesting a defensive role against pathogenic bacteria and potential discovery of novel antibiotics. Overall, this study sheds light on the microbiome’s role in Kellet’s whelk development, emphasizing the significance of host-microbe interactions in vulnerable life history stages. To our knowledge, ours is the first study to use 16S sequencing coupled with RNA sequencing (RNA-seq) to profile the microbiome of an invertebrate PVF.IMPORTANCEThis study provides novel insight to an encapsulated system with strong evidence of symbiosis between the microbial inhabitants and developing host embryos. The Kellet’s whelk perivitelline fluid (PVF) contains microbial organisms of interest that may be providing symbiotic functions and potential antimicrobial properties during this vulnerable life history stage. This study, the first to utilize a comprehensive approach to investigating Kellet’s whelk PVF microbiome, couples 16S rRNA gene long-read sequencing with RNA-seq. This research contributes to and expands our knowledge on the roles of beneficial host-associated microbes.
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spelling doaj.art-19ddea373c9b49508dc91a2df24860592024-03-05T14:04:36ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-03-0112310.1128/spectrum.03514-23Microbiome composition and function within the Kellet’s whelk perivitelline fluidBenjamin N. Daniels0Jenna Nurge1Chanel De Smet2Olivia Sleeper3Crow White4Jean M. Davidson5Pat Fidopiastis6Department of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USADepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USADepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USADepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USADepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USADepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USADepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, California, USAABSTRACTMicrobiomes have gained significant attention in ecological research, owing to their diverse interactions and essential roles within different organismal ecosystems. Microorganisms, such as bacteria, archaea, and viruses, have profound impact on host health, influencing digestion, metabolism, immune function, tissue development, and behavior. This study investigates the microbiome diversity and function of Kellet’s whelk (Kelletia kelletii) perivitelline fluid (PVF), which sustains thousands of developing K. kelletii embryos within a polysaccharide and protein matrix. Our core microbiome analysis reveals a diverse range of bacteria, with the Roseobacter genus being the most abundant. Additionally, genes related to host-microbe interactions, symbiosis, and quorum sensing were detected, indicating a potential symbiotic relationship between the microbiome and Kellet’s whelk embryos. Furthermore, the microbiome exhibits gene expression related to antibiotic biosynthesis, suggesting a defensive role against pathogenic bacteria and potential discovery of novel antibiotics. Overall, this study sheds light on the microbiome’s role in Kellet’s whelk development, emphasizing the significance of host-microbe interactions in vulnerable life history stages. To our knowledge, ours is the first study to use 16S sequencing coupled with RNA sequencing (RNA-seq) to profile the microbiome of an invertebrate PVF.IMPORTANCEThis study provides novel insight to an encapsulated system with strong evidence of symbiosis between the microbial inhabitants and developing host embryos. The Kellet’s whelk perivitelline fluid (PVF) contains microbial organisms of interest that may be providing symbiotic functions and potential antimicrobial properties during this vulnerable life history stage. This study, the first to utilize a comprehensive approach to investigating Kellet’s whelk PVF microbiome, couples 16S rRNA gene long-read sequencing with RNA-seq. This research contributes to and expands our knowledge on the roles of beneficial host-associated microbes.https://journals.asm.org/doi/10.1128/spectrum.03514-23microbiomeRNA-seqantimicrobial activityantibiotic biosynthesisgene expressionGO term
spellingShingle Benjamin N. Daniels
Jenna Nurge
Chanel De Smet
Olivia Sleeper
Crow White
Jean M. Davidson
Pat Fidopiastis
Microbiome composition and function within the Kellet’s whelk perivitelline fluid
Microbiology Spectrum
microbiome
RNA-seq
antimicrobial activity
antibiotic biosynthesis
gene expression
GO term
title Microbiome composition and function within the Kellet’s whelk perivitelline fluid
title_full Microbiome composition and function within the Kellet’s whelk perivitelline fluid
title_fullStr Microbiome composition and function within the Kellet’s whelk perivitelline fluid
title_full_unstemmed Microbiome composition and function within the Kellet’s whelk perivitelline fluid
title_short Microbiome composition and function within the Kellet’s whelk perivitelline fluid
title_sort microbiome composition and function within the kellet s whelk perivitelline fluid
topic microbiome
RNA-seq
antimicrobial activity
antibiotic biosynthesis
gene expression
GO term
url https://journals.asm.org/doi/10.1128/spectrum.03514-23
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