Nepali oral microbiomes reflect a gradient of lifestyles from traditional to industrialized

From BugSigDB
Needs review
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Ryu EP, Gautam Y, Proctor DM, Bhandari D, Tandukar S, Gupta M, Gautam GP, Relman DA, Shibl AA, Sherchand JB, Jha AR, Davenport ER
Journal
Microbiome
Year
2024
Keywords:
Lifestyle, Nepali populations, Oral microbiome, Oral microbiota, Salivary microbiome
BACKGROUND: Lifestyle plays an important role in shaping the gut microbiome. However, its contributions to the oral microbiome remain less clear, due to the confounding effects of geography and methodology in investigations of populations studied to date. Furthermore, while the oral microbiome seems to differ between foraging and industrialized populations, we lack insight into whether transitions to and away from agrarian lifestyles shape the oral microbiota. Given the growing interest in so-called "vanishing microbiomes" potentially being a risk factor for increased disease prevalence in industrialized populations, it is important that we distinguish lifestyle from geography in the study of microbiomes across populations. RESULTS: Here, we investigate salivary microbiomes of 63 Nepali individuals representing a spectrum of lifestyles: foraging, subsistence farming (individuals that transitioned from foraging to farming within the last 50 years), agriculturalists (individuals that have transitioned to farming for at least 300 years), and industrialists (expatriates that immigrated to the USA within the last 20 years). We characterize the role of lifestyle in microbial diversity, identify microbes that differ between lifestyles, and pinpoint specific lifestyle factors that may be contributing to differences in the microbiomes across populations. Contrary to prevailing views, when geography is controlled for, oral microbiome alpha diversity does not differ significantly across lifestyles. Microbiome composition, however, follows the gradient of lifestyles from foraging through agrarianism to industrialism, supporting the notion that lifestyle indeed plays a role in the oral microbiome. Relative abundances of several individual taxa, including Streptobacillus and an unclassified Porphyromonadaceae genus, also mirror lifestyle. Finally, we identify specific lifestyle factors associated with microbiome composition across the gradient of lifestyles, including smoking and grain sources. CONCLUSION: Our findings demonstrate that by studying populations within Nepal, we can isolate an important role of lifestyle in determining oral microbiome composition. In doing so, we highlight the potential contributions of several lifestyle factors, underlining the importance of carefully examining the oral microbiome across lifestyles to improve our understanding of global microbiomes. Video Abstract. सारांश पृष्ठभूमि: मानवको आन्द्रामा ब्याक्टेरिया, भाइरस, फंगस (ढुसी), लगायत अरू विभिन्न प्रकारका सूक्ष्मजीवहरूका समुदाय पाईन्छन्, जसलाई माइक्रोबायोम भनिन्छ। आन्द्रामा हुने माइक्रोबायोमले मानवको पाचन, प्रतिरक्षा प्रणाली, र अन्य शारीरिक प्रक्रियाहरूमा योगदान पुर्याउने हुनाले यिनले मानव स्वास्थ्य र रोगको निर्धारण गर्नमा महत्त्वपूर्ण भूमिका खेल्छन्। त्यसैगरी मानव मुखमा पनि सूक्ष्मजीवहरूका समुदायहरू हुन्छन् जसले दाँत र गिजालाई स्वस्थ राख्नमा योगदान पुर्‍याउँछन्। जीवनशैलीले आन्द्राको माइक्रोबायोमलाई आकार दिन महत्त्वपूर्ण भूमिका खेल्छ। साथै, जङलमा निर्भर भएर प्रकृतिक जीवनशैली जिउने र औध्योगिक्रित भएका मानव समुदायहरुको बीच मुखको माइक्रोबायोममा धेरै भिन्नता देखिन्छ। जङलमा निर्भर भएर प्रकृतिक जीवनशैली जिउने मानव समुदायहरुमा पाईने धेरै सूक्ष्मजीवहरू औद्योगिक जनसमुदायहरुमा मा पाईन छाडिसकेका छन् र यस्ता ‘विलुप्त माइक्रोबायोम’ बिभिन्न रोगहरुका जोखिमका कारक हुन सक्ने हुँदा चासोका बिषय बन्न पुगेका छन्। तथापि, अहिलेसम्मका अनुसन्धानमा जीवनशैलिको परिवर्तन सँगै मुखको माइक्रोबायोममा के कस्ता परिवर्तनहरु आउँछन् भन्ने कुरा स्पष्ट हुन सकेको छैन। विभिन्न जीवनशैली ब्यथीत गर्ने मानिसहरु बीच जीवनशैलीको साथसाथै भौगोलिक भिन्नता पनि हुने गर्दछ। तसर्थ, मनिसहरुका मुखका माईक्रोबायोममा जीवनशैली र भूगोलको असरलाई छुट्याउनु महत्त्वपूर्ण देखिएको छ। परिणामहरू: यहाँ, हामीले ६३ जना नेपाली व्यक्तिको थुक संकलन गरेर मुखका माइक्रोबायोमको अनुसन्धान गर्यौं। हाम्रो अध्ययनमा संलग्न भएका ब्यक्तिहरुले विभिन्न जीवनशैलीको प्रतिनिधित्व गर्छन्: जङलमा निर्भर भएर प्रकृतिक जीवनशैली जिउने, जङलबाट कृषितर्फ हालसालै परिवर्तन भएका (अन्तिम ५० वर्ष भित्र), कृषक (बिगतका ३०० वर्ष भन्दा बढी समयदेखि कृषिमा संलग्न भएका), र औद्योगिक (अन्तिम २० वर्ष भित्र संयुक्त राज्य अमेरिका मा आप्रवासन गरेका नेपालीहरु)। हामीले यस् अध्ययनमा जीवनशैलीले मुखका माईक्रोबायोमको विविधतामा कसरी योगदान पुर्याउँछन् भन्ने कुरको विश्लेषण गरेका छौं, जीवनशैलीहरू बीच फरक पर्ने सूक्ष्मजीवहरूको पहिचान गरेका छौं, र माइक्रोबायोममा फरक पार्ने कारकहरूको पहिचान गरेका छौं। प्रचलित दृष्टिकोणहरू विपरीत, भूगोललाई नियन्त्रण गर्दा, बिभिन्न जीवनशैलीहरू बीच मुखको माइक्रोबायोममा हुने सूक्ष्मजीवहरूको सन्ख्या (अल्फा विविधता) मा धेरै फरक देखिएन, तर मुखको माइक्रोबायोमको संरचना भने जीवनशैलीको क्रमिक चरणसँग मिल्दोजुल्दो देखियो, जसले देखाउँछ कि जीवनशैलीले मुखको माइक्रोबायोममा को संरचना निर्धारण गर्न एउटा प्रमुख भूमिका खेल्दछ। स्ट्रेप्टोबासिलस र असम्प्रेषित पोरफिरोमोनाडासिए जीनस सहितका केही सूक्ष्मजीवहरूको सापेक्ष सापेक्षिक प्रचुरता पनि जीवनशैलीसँग मेल खाने हामीले यस् अध्ययनबाट थाहा पाएका छौं। अन्ततः, हामीले जीवनशैलीको क्रमिक चरणमा माइक्रोबायोम संरचनासँग सम्बन्धित विशिष्ट जीवनशैलीसँग आबद्ध हुने धूम्रपान र अनाज जस्ता कारकहरूको पहिचान गरेका छौं। निष्कर्ष: हाम्रा निष्कर्षहरूले प्रष्ट परेका छन कि भूगोललाई नियन्त्रण गर्दा, हाम्रो जीवनशैलीले हाम्रा मुखको माइक्रोबायोमको संरचना निर्धारण गर्ने महत्त्वपूर्ण भूमिका खेल्दो रहेछ। यस् अध्ययनले मानव समुदायहरुमा मुखको माइक्रोबायोमको अध्ययन गरेमा माइक्रोबायोमबारेको हाम्रो बुझाइमा सुधार ल्याउन सकिने पनि देखाउँछ। बढ्दो शहरीकरण सँगसँगै नेपालीहरुको माइक्रोबायोममा परिवर्तन हुँदै गरेको र यस्ता परिवर्तनहरुले नेपालीहरुमा बिभिन्न दीर्घकालीन रोगहरुको व्यापकता बढाउन सक्ने हुनाले यस् सम्बन्धमा उपर्योक्त निकायहरुको ध्यानाकर्षण हुनुपर्ने आवश्यकता पनि यस् अध्ययनले प्रष्ट पारेको छ।.

Experiment 1


Needs review

Curated date: 2024/11/24

Curator: Tosin

Revision editor(s): Tosin

Subjects

Location of subjects
Nepal
United States of America
Host species Species from which microbiome was sampled. Contact us to have more species added.
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Lifestyle measurement Lifestyle measurement,lifestyle measurement
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Combination of Foragers, recently settled, agriculturalists, expats.
Group 1 name Corresponds to the case (exposed) group for case-control studies
American Industrial
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Expatriates that immigrated to the USA within the last 20 years.
Group 0 sample size Number of subjects in the control (unexposed) group
85
Group 1 sample size Number of subjects in the case (exposed) group
6
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
Current antibiotic use

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V4
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
relative abundances
Statistical test
Linear Regression
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.05
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
sex


Signature 1

Needs review

Curated date: 2024/11/24

Curator: Tosin

Revision editor(s): Tosin

Source: Figure 4

Description: Abundances of genera significantly following the lifestyle gradient ordered from most traditional (foragers) to most industrialized (American industrialists), left to right.

Abundance in Group 1: increased abundance in American Industrial

NCBI Quality ControlLinks
Atopobium

Revision editor(s): Tosin

Signature 2

Needs review

Curated date: 2024/11/24

Curator: Tosin

Revision editor(s): Tosin

Source: Figure 4

Description: Abundances of genera significantly following the lifestyle gradient ordered from most traditional (foragers) to most industrialized (American industrialists), left to right.

Abundance in Group 1: decreased abundance in American Industrial

NCBI Quality ControlLinks
Granulicatella
Moraxella
Neisseria
Simonsiella
Streptobacillus
unclassified Bacteroidota
unclassified Porphyromonadaceae

Revision editor(s): Tosin

Experiment 2


Needs review

Curated date: 2024/11/24

Curator: Tosin

Revision editor(s): Tosin

Differences from previous experiment shown

Subjects

Location of subjects
Nepal


Group 0 name Corresponds to the control (unexposed) group for case-control studies
Wheat/Rice
Group 1 name Corresponds to the case (exposed) group for case-control studies
Barley/Maize
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Barley/Maize a grain type considered as a lifestyle factor associated with the oral microbiome of individuals.
Group 0 sample size Number of subjects in the control (unexposed) group
Not specified
Group 1 sample size Number of subjects in the case (exposed) group
Not specified

Lab analysis

Statistical Analysis

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
age, sex


Signature 1

Needs review

Curated date: 2024/11/24

Curator: Tosin

Revision editor(s): Tosin

Source: Figure 5B, 5C

Description: Grain, a lifestyle factor associated with significant individual oral genera.

Abundance in Group 1: increased abundance in Barley/Maize

NCBI Quality ControlLinks
Brachymonas

Revision editor(s): Tosin

Experiment 3


Needs review

Curated date: 2024/11/26

Curator: Tosin

Revision editor(s): Tosin

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-smokers
Group 1 name Corresponds to the case (exposed) group for case-control studies
Smokers
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Individuals engaged in smoking

Lab analysis

Statistical Analysis

Statistical test
T-Test


Signature 1

Needs review

Curated date: 2024/11/27

Curator: Tosin

Revision editor(s): Tosin

Source: S11A

Description: Differentially abundant taxa between smokers and Non-smokers group

Abundance in Group 1: increased abundance in Smokers

NCBI Quality ControlLinks
Atopobium

Revision editor(s): Tosin

Signature 2

Needs review

Curated date: 2024/11/27

Curator: Tosin

Revision editor(s): Tosin

Source: Figure S11A

Description: Differentially abundant taxa between smokers and Non-smokers group.

Abundance in Group 1: decreased abundance in Smokers

NCBI Quality ControlLinks
Granulicatella
unclassified Porphyromonadaceae
Neisseria

Revision editor(s): Tosin

Experiment 4


Needs review

Curated date: 2024/11/27

Curator: Tosin

Revision editor(s): Tosin

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-sinsu consumers
Group 1 name Corresponds to the case (exposed) group for case-control studies
Sinsu comsumers
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Individuals that consume sinsu.

Lab analysis

Statistical Analysis

Signature 1

Needs review

Curated date: 2024/11/27

Curator: Tosin

Revision editor(s): Tosin

Source: Figure S11B

Description: Differentially abundant taxa between non-sinsu consumers and sinsu consumers.

Abundance in Group 1: increased abundance in Sinsu comsumers

NCBI Quality ControlLinks
Brachymonas
Moraxella
unclassified Porphyromonadaceae

Revision editor(s): Tosin

Experiment 5


Needs review

Curated date: 2024/11/27

Curator: Tosin

Revision editor(s): Tosin

Differences from previous experiment shown

Subjects

Location of subjects
Nepal
United States of America


Group 0 name Corresponds to the control (unexposed) group for case-control studies
Traditional populations
Group 1 name Corresponds to the case (exposed) group for case-control studies
Industrialized populations
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
American industrialists and Expats were categorized as Industralized populations.
Group 0 sample size Number of subjects in the control (unexposed) group
73
Group 1 sample size Number of subjects in the case (exposed) group
18

Lab analysis

Statistical Analysis

Statistical test
Kruskall-Wallis
Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
sex


Signature 1

Needs review

Curated date: 2024/11/27

Curator: Tosin

Revision editor(s): Tosin

Source: Figure S16B

Description: Abundance of Fusobacterium contributing to platinum resistance significantly differs between the traditional and industrialized populations.

Abundance in Group 1: decreased abundance in Industrialized populations

NCBI Quality ControlLinks
Fusobacterium

Revision editor(s): Tosin

Experiment 6


Needs review

Curated date: 2024/11/28

Curator: Tosin

Revision editor(s): Tosin

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Combination of Foragers, recently settled, agriculturalists, expats.
Group 1 name Corresponds to the case (exposed) group for case-control studies
American Industrial
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Expatriates that immigrated to the USA within the last 20 years.
Group 0 sample size Number of subjects in the control (unexposed) group
85
Group 1 sample size Number of subjects in the case (exposed) group
6

Lab analysis

Statistical Analysis

Signature 1

Needs review

Curated date: 2024/11/28

Curator: Tosin

Revision editor(s): Tosin

Source: Figure 4

Description: Abundances of genera significantly following the lifestyle gradient ordered from most traditional (foragers) to most industrialized (American industrialists), left to right.

Abundance in Group 1: decreased abundance in American Industrial

NCBI Quality ControlLinks
Streptobacillus
unclassified Porphyromonadaceae

Revision editor(s): Tosin