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Deciphering Diversity Indices for a Better Understanding of Microbial Communities

  • Kim, Bo-Ra (Department of Animal Resources Science, Dankook University) ;
  • Shin, Jiwon (Department of Animal Resources Science, Dankook University) ;
  • Guevarra, Robin B. (Department of Animal Resources Science, Dankook University) ;
  • Lee, Jun Hyung (Department of Animal Resources Science, Dankook University) ;
  • Kim, Doo Wan (National Institute of Animal Science, Rural Development Administration) ;
  • Seol, Kuk-Hwan (National Institute of Animal Science, Rural Development Administration) ;
  • Lee, Ju-Hoon (Department of Food Science and Biotechnology, Institute of Life Science and Resources, Kyung Hee University) ;
  • Kim, Hyeun Bum (Department of Animal Resources Science, Dankook University) ;
  • Isaacson, Richard E. (Department of Veterinary and Biomedical Sciences, University of Minnesota)
  • Received : 2017.09.14
  • Accepted : 2017.10.12
  • Published : 2017.12.28

Abstract

The past decades have been a golden era during which great tasks were accomplished in the field of microbiology, including food microbiology. In the past, culture-dependent methods have been the primary choice to investigate bacterial diversity. However, using culturein-dependent high-throughput sequencing of 16S rRNA genes has greatly facilitated studies exploring the microbial compositions and dynamics associated with health and diseases. These culture-independent DNA-based studies generate large-scale data sets that describe the microbial composition of a certain niche. Consequently, understanding microbial diversity becomes of greater importance when investigating the composition, function, and dynamics of the microbiota associated with health and diseases. Even though there is no general agreement on which diversity index is the best to use, diversity indices have been used to compare the diversity among samples and between treatments with controls. Tools such as the Shannon-Weaver index and Simpson index can be used to describe population diversity in samples. The purpose of this review is to explain the principles of diversity indices, such as Shannon-Weaver and Simpson, to aid general microbiologists in better understanding bacterial communities. In this review, important questions concerning microbial diversity are addressed. Information from this review should facilitate evidence-based strategies to explore microbial communities.

Keywords

References

  1. Berg RD. 1996. The indigenous gastrointestinal microflora. Trends Microbiol. 4: 430-435. https://doi.org/10.1016/0966-842X(96)10057-3
  2. Manson JM, Rauch M, Gilmore MS. 2008. The commensal microbiology of the gastrointestinal tract. Adv. Exp. Med. Biol. 635: 15-28.
  3. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, et al. 2003. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299: 2074-2076. https://doi.org/10.1126/science.1080029
  4. Sonnenburg JL, Angenent LT, Gordon JI. 2004. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat. Immun. 5: 569-573. https://doi.org/10.1038/ni1079
  5. Kim HB, Isaacson RE. 2015. The pig gut microbial diversity: understanding the pig gut microbial ecology through the next generation high throughput sequencing. Vet. Microbiol. 177: 242-251. https://doi.org/10.1016/j.vetmic.2015.03.014
  6. Isaacson R, Kim HB. 2012. The intestinal microbiome of the pig. Anim. Health Res. Rev. 13: 100-109. https://doi.org/10.1017/S1466252312000084
  7. Schmalenberger A, Schwieger F, Tebbe CC. 2001. Effect of primers hybridizing to different evolutionarily conserved regions of the small-subunit rRNA gene in PCR-based microbial community analyses and genetic profiling. Appl. Environ. Microbiol. 67: 3557-3563. https://doi.org/10.1128/AEM.67.8.3557-3563.2001
  8. Chakravorty S, Helb D, Burday M, Connell N, Alland D. 2007. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods 69: 330-339. https://doi.org/10.1016/j.mimet.2007.02.005
  9. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, et al. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl. Acad. Sci. USA 103: 12115-12120. https://doi.org/10.1073/pnas.0605127103
  10. Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA, et al. 2007. Microbial population structures in the deep marine biosphere. Science 318: 97-100. https://doi.org/10.1126/science.1146689
  11. Highlander SK. 2012. High throughput sequencing methods for microbiome profiling: application to food animal systems. Anim. Health Res. Rev. 13: 40-53. https://doi.org/10.1017/S1466252312000126
  12. Sanschagrin S, Yergeau E. 2014. Next-generation sequencing of 16S ribosomal RNA gene amplicons. J. Vis. Exp. DOI: 10.3791/51709.
  13. Schloss PD, Handelsman J. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71: 1501-1506. https://doi.org/10.1128/AEM.71.3.1501-1506.2005
  14. Schloss PD, Handelsman J. 2006. Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures. Appl. Environ. Microbiol. 72: 6773-6779. https://doi.org/10.1128/AEM.00474-06
  15. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  16. Chao A. 1984. Non-parametric estimation of the number of classes in a population. Scand. J. Stat. 11: 265-270.
  17. Chao A, Bunge J. 2002. Estimating the number of species in a stochastic abundance model. Biometrics 58: 531-539. https://doi.org/10.1111/j.0006-341X.2002.00531.x
  18. Chao A, Chazdon RL, Colwell RK, Shen TJ. 2006. Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62: 361-371. https://doi.org/10.1111/j.1541-0420.2005.00489.x
  19. Hughes JB, Bohannan BJM. 2004. Application of ecological diversity statistics in microbial ecology. Mol. Microb. Ecol. Manual 7.01: 1321-1344.
  20. Haegeman B, Hamelin J, Moriarty J, Neal P, Dushoff J, Weitz JS. 2013. Robust estimation of microbial diversity in theory and in practice. ISME J. 7: 1092-1101. https://doi.org/10.1038/ismej.2013.10
  21. Lemos LN, Fulthorpe RR, Triplett EW, Roesch LF. 2011. Rethinking microbial diversity analysis in the high throughput sequencing era. J. Microbiol. Methods 86: 42-51. https://doi.org/10.1016/j.mimet.2011.03.014
  22. Magurran A. 2004. Measuring Biological Diversity. Blackwell Science Ltd, Oxford, United Kingdom.
  23. Simpson EH. 1949. Measurement of diversity. Nature 163: 688. https://doi.org/10.1038/163688a0
  24. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJ. 2001. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol. 67: 4399-4406. https://doi.org/10.1128/AEM.67.10.4399-4406.2001
  25. Sanders HL. 1969. Benthic marine diversity and the stability-time hypothesis. Brookhaven Symp. Biol. 22: 71-81.
  26. Efron B, Tibshirani R. 1993. An Introduction to the Bootsrap. Chapman & Hall, New York.
  27. Shen TJ, Chao A, Ling C. 2003. Predicting the number of new species in further taxonomic sampling. Ecology 84: 798-804. https://doi.org/10.1890/0012-9658(2003)084[0798:PTNONS]2.0.CO;2
  28. Chao A, Lee S. 1992. Estimating the number of classes via sample coverage. J. Am. Stat. Assoc. 87: 210-217. https://doi.org/10.1080/01621459.1992.10475194
  29. Chao A, Ma M, Yang M. 1993. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 80: 193-201. https://doi.org/10.1093/biomet/80.1.193
  30. Sornplang P, Piyadeatsoontorn S. 2016. Probiotic isolates from unconventional sources: a review. J. Anim. Sci. Technol. 58: 26. https://doi.org/10.1186/s40781-016-0108-2

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  98. Short- and Branched-Chain Fatty Acids as Fecal Markers for Microbiota Activity in Vegans and Omnivores vol.13, pp.6, 2017, https://doi.org/10.3390/nu13061808
  99. Comparison of bacterial communities in roots of selected trees with and without summer truffle (Tuber aestivum) ectomycorrhiza vol.63, pp.2, 2017, https://doi.org/10.2478/ffp-2021-0011
  100. Environmental influences shaping microbial communities in a low oxygen, highly stratified marine embayment vol.87, pp.None, 2017, https://doi.org/10.3354/ame01978
  101. Associations of fine particulate matter and its constituents with airway inflammation, lung function, and buccal mucosa microbiota in children vol.773, pp.None, 2017, https://doi.org/10.1016/j.scitotenv.2021.145619
  102. Influence of Intramuscular Depot Medroxyprogesterone Acetate Initiation on Vaginal Microbiota in the Postpartum Period vol.72, pp.12, 2017, https://doi.org/10.1093/cid/ciaa1876
  103. Microbial communities of biofilms developed in a chlorinated drinking water distribution system: A field study of antibiotic resistance and biodiversity vol.774, pp.None, 2017, https://doi.org/10.1016/j.scitotenv.2021.145113
  104. Live and ultrasound-inactivated Lacticaseibacillus casei modulate the intestinal microbiota and improve biochemical and cardiovascular parameters in male rats fed a high-fat diet vol.12, pp.12, 2017, https://doi.org/10.1039/d1fo01064f
  105. Association of Diverse Staphylococcus aureus Populations with Pseudomonas aeruginosa Coinfection and Inflammation in Cystic Fibrosis Airway Infection vol.6, pp.3, 2021, https://doi.org/10.1128/msphere.00358-21
  106. Gut microbiome, body weight, and mammographic breast density in healthy postmenopausal women vol.32, pp.7, 2021, https://doi.org/10.1007/s10552-021-01420-6
  107. Using next‐generation sequencing to detect oral microbiome change following periodontal interventions: A systematic review vol.27, pp.5, 2017, https://doi.org/10.1111/odi.13405
  108. Effect of Fungicide Application on Lowbush Blueberries Soil Microbiome vol.9, pp.7, 2017, https://doi.org/10.3390/microorganisms9071366
  109. Evaluation of combined anaerobic membrane bioreactor and downflow hanging sponge reactor for treatment of synthetic textile wastewater vol.9, pp.4, 2017, https://doi.org/10.1016/j.jece.2021.105276
  110. Commensal microbiota contributes to predicting the response to immune checkpoint inhibitors in non‐small‐cell lung cancer patients vol.112, pp.8, 2021, https://doi.org/10.1111/cas.14979
  111. Seasonal Variability of the Airborne Eukaryotic Community Structure at a Coastal Site of the Central Mediterranean vol.13, pp.8, 2021, https://doi.org/10.3390/toxins13080518
  112. Microbial communities of poultry house dust, excreta and litter are partially representative of microbiota of chicken caecum and ileum vol.16, pp.8, 2017, https://doi.org/10.1371/journal.pone.0255633
  113. Variations in the Community Structure of Fungal Microbiota Associated with Apple Fruit Shaped by Fruit Bagging-Based Practice vol.7, pp.9, 2017, https://doi.org/10.3390/jof7090764
  114. Subacute Exposure to an Environmentally Relevant Dose of Di-(2-ethylhexyl) Phthalate during Gestation Alters the Cecal Microbiome, but Not Pregnancy Outcomes in Mice vol.9, pp.9, 2017, https://doi.org/10.3390/toxics9090215
  115. Identification & correlation of bacterial diversity in oral cancer and long-term tobacco chewers- A case-control pilot study vol.70, pp.9, 2017, https://doi.org/10.1099/jmm.0.001417
  116. Eight‐week exercise training in humans with obesity: Marked improvements in insulin sensitivity and modest changes in gut microbiome vol.29, pp.10, 2021, https://doi.org/10.1002/oby.23252
  117. Microbiota profile in mesophilic biodigestion of sugarcane vinasse in batch reactors vol.84, pp.8, 2017, https://doi.org/10.2166/wst.2021.375
  118. Antibiotics accelerate growth at the expense of immunity vol.288, pp.1961, 2017, https://doi.org/10.1098/rspb.2021.1819
  119. Effects of Recreational Boating on Microbial and Meiofauna Diversity in Coastal Shallow Ecosystems of the Baltic Sea vol.6, pp.5, 2017, https://doi.org/10.1128/msphere.00127-21
  120. Isoquinoline alkaloids induce partial protection of laying hens from the impact of Campylobacter hepaticus (spotty liver disease) challenge vol.100, pp.11, 2021, https://doi.org/10.1016/j.psj.2021.101423
  121. Mango Endophyte and Epiphyte Microbiome Composition during Fruit Development and Post-Harvest Stages vol.7, pp.11, 2021, https://doi.org/10.3390/horticulturae7110495
  122. Diversity and Hydrocarbon-Degrading Potential of Deep-Sea Microbial Community from the Mid-Atlantic Ridge, South of the Azores (North Atlantic Ocean) vol.9, pp.11, 2021, https://doi.org/10.3390/microorganisms9112389
  123. Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors vol.15, pp.12, 2021, https://doi.org/10.1002/1878-0261.13070
  124. Microplastics habituated with biofilm change decabrominated diphenyl ether degradation products and thyroid endocrine toxicity vol.228, pp.None, 2017, https://doi.org/10.1016/j.ecoenv.2021.112991
  125. Tuber flours improve intestinal health and modulate gut microbiota composition vol.12, pp.None, 2021, https://doi.org/10.1016/j.fochx.2021.100145
  126. Metagenomic analysis of MWWTP effluent treated via solar photo-Fenton at neutral pH: Effects upon microbial community, priority pathogens, and antibiotic resistance genes vol.801, pp.None, 2017, https://doi.org/10.1016/j.scitotenv.2021.149599
  127. Vaginal microbiome topic modeling of laboring Ugandan women with and without fever vol.7, pp.1, 2017, https://doi.org/10.1038/s41522-021-00244-1
  128. Linking prokaryotic community composition to carbon biogeochemical cycling across a tropical peat dome in Sarawak, Malaysia vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-81865-6
  129. Long term impact of vonoprazan‐based Helicobacter pylori treatment on gut microbiota and its relation to post‐treatment body weight changes vol.26, pp.6, 2017, https://doi.org/10.1111/hel.12851
  130. Individual differences in behaviour and gut bacteria are associated in collared peccary (Mammalia, Tayassuidae) vol.131, pp.6, 2017, https://doi.org/10.1111/jam.15133
  131. Zebrafish, Danio rerio , Skin Mucus Harbors a Distinct Bacterial Community Dominated by Actinobacteria vol.18, pp.6, 2021, https://doi.org/10.1089/zeb.2021.0040
  132. The influence of prior experience on food preference by sheep exposed to unfamiliar feeds and flavors vol.246, pp.None, 2017, https://doi.org/10.1016/j.applanim.2021.105530
  133. Oxidized phospholipids cause changes in jejunum mucus that induce dysbiosis and systemic inflammation vol.63, pp.1, 2017, https://doi.org/10.1016/j.jlr.2021.100153
  134. The Diversity, Metabolomics Profiling, and the Pharmacological Potential of Actinomycetes Isolated from the Estremadura Spur Pockmarks (Portugal) vol.20, pp.1, 2017, https://doi.org/10.3390/md20010021
  135. Metagenomic community composition and resistome analysis in a full-scale cold climate wastewater treatment plant vol.17, pp.None, 2017, https://doi.org/10.1186/s40793-022-00398-1
  136. Microbiome shifts in sprouts (alfalfa, radish, and rapeseed) during production from seed to sprout using 16S rRNA microbiome sequencing vol.152, pp.None, 2017, https://doi.org/10.1016/j.foodres.2021.110896
  137. Dietary tryptophan, tyrosine, and phenylalanine depletion induce reduced food intake and behavioral alterations in mice vol.244, pp.None, 2017, https://doi.org/10.1016/j.physbeh.2021.113653
  138. Performance and recovery of nitrifying biofilm after exposure to prolonged starvation vol.290, pp.None, 2017, https://doi.org/10.1016/j.chemosphere.2021.133323
  139. Exploring the relationship between the gut microbiome and mental health outcomes in a posttraumatic stress disorder cohort relative to trauma-exposed controls vol.56, pp.None, 2022, https://doi.org/10.1016/j.euroneuro.2021.11.009