Comprehensive functional core microbiome comparison in genetically obese and lean hosts under the same environment

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Abstract

Our study provides an exhaustive comparison of the microbiome core functionalities (captured by 3,936 microbial gene abundances) between hosts with divergent genotypes for intramuscular lipid deposition. After 10 generations of divergent selection for intramuscular fat in rabbits and 4.14 phenotypic standard deviations (SD) of selection response, we applied a combination of compositional and multivariate statistical techniques to identify 122 cecum microbial genes with differential abundances between the lines (ranging from −0.75 to +0.73 SD). This work elucidates that microbial biosynthesis lipopolysaccharides, peptidoglycans, lipoproteins, mucin components, and NADH reductases, amongst others, are influenced by the host genetic determination for lipid accretion in muscle. We also differentiated between host-genetically influenced microbial mechanisms regulating lipid deposition in body or intramuscular reservoirs, with only 28 out of 122 MGs commonly contributing to both. Importantly, the results of this study are of relevant interest for the efficient development of strategies fighting obesity.

Abstract

Martínez-Álvaro et al. employ metagenomic sequencing to compare the differences in caecum microbiome between lean and genetically obese rabbits exhibiting different levels of intramuscular fat. Lipid aggregation in muscle can be attributed to host genetic interactions with microbial biosynthetic products.

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Fast and sensitive protein alignment using DIAMOND.

Benjamin Buchfink, Chao Xie, Daniel Huson (2015)

The alignment of sequencing reads against a protein reference database is a major computational bottleneck in metagenomics and data-intensive evolutionary projects. Although recent tools offer improved performance over the gold standard BLASTX, they exhibit only a modest speedup or low sensitivity. We introduce DIAMOND, an open-source algorithm based on double indexing that is 20,000 times faster than BLASTX on short reads and has a similar degree of sensitivity.

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An obesity-associated gut microbiome with increased capacity for energy harvest.

Peter J Turnbaugh, Ruth E Ley, Michael A Mahowald … (2006)

The worldwide obesity epidemic is stimulating efforts to identify host and environmental factors that affect energy balance. Comparisons of the distal gut microbiota of genetically obese mice and their lean littermates, as well as those of obese and lean human volunteers have revealed that obesity is associated with changes in the relative abundance of the two dominant bacterial divisions, the Bacteroidetes and the Firmicutes. Here we demonstrate through metagenomic and biochemical analyses that these changes affect the metabolic potential of the mouse gut microbiota. Our results indicate that the obese microbiome has an increased capacity to harvest energy from the diet. Furthermore, this trait is transmissible: colonization of germ-free mice with an 'obese microbiota' results in a significantly greater increase in total body fat than colonization with a 'lean microbiota'. These results identify the gut microbiota as an additional contributing factor to the pathophysiology of obesity.

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Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19·2 million participants

Emily Sonestedt, Kim Overvad (2016)

Summary Background Underweight and severe and morbid obesity are associated with highly elevated risks of adverse health outcomes. We estimated trends in mean body-mass index (BMI), which characterises its population distribution, and in the prevalences of a complete set of BMI categories for adults in all countries. Methods We analysed, with use of a consistent protocol, population-based studies that had measured height and weight in adults aged 18 years and older. We applied a Bayesian hierarchical model to these data to estimate trends from 1975 to 2014 in mean BMI and in the prevalences of BMI categories (<18·5 kg/m2 [underweight], 18·5 kg/m2 to <20 kg/m2, 20 kg/m2 to <25 kg/m2, 25 kg/m2 to <30 kg/m2, 30 kg/m2 to <35 kg/m2, 35 kg/m2 to <40 kg/m2, ≥40 kg/m2 [morbid obesity]), by sex in 200 countries and territories, organised in 21 regions. We calculated the posterior probability of meeting the target of halting by 2025 the rise in obesity at its 2010 levels, if post-2000 trends continue. Findings We used 1698 population-based data sources, with more than 19·2 million adult participants (9·9 million men and 9·3 million women) in 186 of 200 countries for which estimates were made. Global age-standardised mean BMI increased from 21·7 kg/m2 (95% credible interval 21·3–22·1) in 1975 to 24·2 kg/m2 (24·0–24·4) in 2014 in men, and from 22·1 kg/m2 (21·7–22·5) in 1975 to 24·4 kg/m2 (24·2–24·6) in 2014 in women. Regional mean BMIs in 2014 for men ranged from 21·4 kg/m2 in central Africa and south Asia to 29·2 kg/m2 (28·6–29·8) in Polynesia and Micronesia; for women the range was from 21·8 kg/m2 (21·4–22·3) in south Asia to 32·2 kg/m2 (31·5–32·8) in Polynesia and Micronesia. Over these four decades, age-standardised global prevalence of underweight decreased from 13·8% (10·5–17·4) to 8·8% (7·4–10·3) in men and from 14·6% (11·6–17·9) to 9·7% (8·3–11·1) in women. South Asia had the highest prevalence of underweight in 2014, 23·4% (17·8–29·2) in men and 24·0% (18·9–29·3) in women. Age-standardised prevalence of obesity increased from 3·2% (2·4–4·1) in 1975 to 10·8% (9·7–12·0) in 2014 in men, and from 6·4% (5·1–7·8) to 14·9% (13·6–16·1) in women. 2·3% (2·0–2·7) of the world’s men and 5·0% (4·4–5·6) of women were severely obese (ie, have BMI ≥35 kg/m2). Globally, prevalence of morbid obesity was 0·64% (0·46–0·86) in men and 1·6% (1·3–1·9) in women. Interpretation If post-2000 trends continue, the probability of meeting the global obesity target is virtually zero. Rather, if these trends continue, by 2025, global obesity prevalence will reach 18% in men and surpass 21% in women; severe obesity will surpass 6% in men and 9% in women. Nonetheless, underweight remains prevalent in the world’s poorest regions, especially in south Asia. Funding Wellcome Trust, Grand Challenges Canada.

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Author and article information

Contributors

Marina Martínez-Álvaro:

ORCID: http://orcid.org/0000-0003-2295-5839

marina.alvaro@sruc.ac.uk

Agustín Blasco:

ORCID: http://orcid.org/0000-0003-3558-0810

ablasco@dca.upv.es

Journal

Journal ID (nlm-ta): Commun Biol

Journal ID (iso-abbrev): Commun Biol

Title: Communications Biology

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2399-3642

Publication date (Electronic): 1 November 2021

Publication date PMC-release: 1 November 2021

Publication date Collection: 2021

Volume: 4

Electronic Location Identifier: 1246

Affiliations

[1 ]GRID grid.426884.4, ISNI 0000 0001 0170 6644, Scotland´s Rural College, ; Edinburgh, UK

[2 ]GRID grid.157927.f, ISNI 0000 0004 1770 5832, Universitat Politècnica de València, ; Valencia, Spain

[3 ]GRID grid.5612.0, ISNI 0000 0001 2172 2676, Universitat Pompeu Fabra, ; Barcelona, Spain

Author information

Marina Martínez-Álvaro http://orcid.org/0000-0003-2295-5839

Agostina Zubiri-Gaitán http://orcid.org/0000-0001-9254-2461

Pilar Hernández http://orcid.org/0000-0001-7857-7334

Michael Greenacre http://orcid.org/0000-0002-0054-3131

Agustín Blasco http://orcid.org/0000-0003-3558-0810

Article

Publisher ID: 2784

DOI: 10.1038/s42003-021-02784-w

PMC ID: 8560826

PubMed ID: 34725460

SO-VID: e9548b64-0881-4650-b9ad-bf14a5f5b7a1

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 13 June 2021

Date accepted : 11 October 2021

Funding

Funded by: FundRef https://doi.org/10.13039/501100003359, Generalitat Valenciana (Regional Government of Valencia);

Award ID: APOSTD/2017/060

Award Recipient : Marina Martínez-Álvaro

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Keywords: genetics,genetic association study

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Keywords: genetics, genetic association study

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Comprehensive functional core microbiome comparison in genetically obese and lean hosts under the same environment

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Most cited references 99

Fast and sensitive protein alignment using DIAMOND.

An obesity-associated gut microbiome with increased capacity for energy harvest.

Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19·2 million participants

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Cited by 6

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