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Thanatomicrobiome and epinecrotic community signatures for estimation of post-mortem time interval in human cadaver - Applied Microbiology and Biotechnology

  • ️Das, Surajit
  • ️Thu Oct 01 2020

  • Abad Santos J (2019) Decomposition of pig carcasses at varying room temperature. Themis 7:3

    Google Scholar 

  • Adserias-Garriga J, Hernández M, Quijada NM, Rodríguez Lázaro D, Steadman D, Garcia-Gil J (2017a) Daily thanatomicrobiome changes in soil as an approach of postmortem interval estimation: an ecological perspective. Forensic Sci Int 278:388–395. https://doi.org/10.1016/j.forsciint.2017.07.017

    Article  Google Scholar 

  • Adserias-Garriga J, Quijada NM, Hernandez M, Rodríguez Lázaro D, Steadman D, Garcia-Gil LJ (2017b) Dynamics of the oral microbiota as a tool to estimate time since death. Mol Oral Microbiol 32:511–516. https://doi.org/10.1111/omi.12191

    Article  CAS  Google Scholar 

  • Agans R, Gordon A, Kramer DL, Perez-Burillo S, Rufián-Henares JA, Paliy O (2018) Dietary fatty acids sustain the growth of the human gut microbiota. Appl Environ Microbiol 84:e01525–e01518. https://doi.org/10.1128/AEM.01525-18

    Article  CAS  Google Scholar 

  • Ahmed S, Macfarlane GT, Fite A, McBain AJ, Gilbert P, Macfarlane S (2007) Mucosa-associated bacterial diversity in relation to human terminal ileum and colonic biopsy samples. Appl Environ Microbiol 73:7435–7442. https://doi.org/10.1128/AEM.01143-07

    Article  CAS  Google Scholar 

  • Al-Qahtni AH, Mashaly AM, Alajmi RA, Alshehri AA, Al-Musawi ZA, Al-Khalifa MS (2019) Forensic insects attracted to human cadavers in a vehicular environment in Riyadh, Saudi Arabia. Saudi J Biol Sci 26:1499–1502. https://doi.org/10.1016/j.sjbs.2019.04.011

    Article  Google Scholar 

  • Aly R (1996) Microbial infections of skin and nails. In: Baron S (ed) Medical Microbiology, 4th edn. University of Texas Medical Branch at Galveston, Galveston (TX) Chapter 98

    Google Scholar 

  • Amabebe E, Anumba DOC (2018) Thevaginal microenvironment: the physiologic role of Lactobacilli. Front Med 5. https://doi.org/10.3389/fmed.2018.00181

  • Barton W, O'Sullivan O, Cotter PD (2019) Metabolic phenotyping of the human microbiome. F1000Res 8:1956. https://doi.org/10.12688/f1000research.19481.1

    Article  CAS  Google Scholar 

  • Bell CR, Wilkinson JE, Robertson BK, Javan GT (2018) Sex-related differences in the thanatomicrobiome in postmortem heart samples using bacterial gene regions V1-2 and V4. Lett Appl Microbiol 67:144–153. https://doi.org/10.1111/lam.13005

    Article  CAS  Google Scholar 

  • Benbow ME, Barton PS, Ulyshen MD, Beasley JC, DeVault TL, Strickland MS, Tomberlin JK, Jordan HR, Pechal JL (2018) Necrobiome framework for bridging decomposition ecology of autotrophically and heterotrophically derived organic matter. Ecol Monogr 89:e01331. https://doi.org/10.1002/ecm.1331

    Article  Google Scholar 

  • Benbow ME, Lewis AJ, Tomberlin JK, Pechal JL (2013) Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. J Med Entomol 50:440–450. https://doi.org/10.1603/me12194

    Article  CAS  Google Scholar 

  • Benbow ME, Pechal JL, Lang JM, Erb R, Wallace JR (2015) The potential of high-throughput metagenomic sequencing of aquatic bacterial communities to estimate the postmortem submersion interval. J Forensic Sci 60:1500–1510. https://doi.org/10.1111/1556-4029.12859

    Article  Google Scholar 

  • Booijink CCGM, Zoetendal EG, Kleerebezem M, de Vos WM (2007) Micobial communities in the human small intestine: coupling diversity to metagenomics. Fut Micobiol 2:285–295. https://doi.org/10.2217/17460913.2.3.285

    Article  CAS  Google Scholar 

  • Bornside GH, Welsh JS, Cohn I Jr (1966) Bacterial flora of the human small intestine. JAMA 196:1125–1127. https://doi.org/10.1001/jama.1966.03100260063018

    Article  CAS  Google Scholar 

  • Brackett E (2018) Thanatomicrobiome signatures in drug overdose cases. Thesis presented to the Honors College of Middle Tennessee State University. https://jewlscholar.mtsu.edu/bitstream/handle/mtsu/5596/BRACKETT%20Final%20Thesis.pdf?sequence=1&isAllowed=y.

  • Burcham ZM, Hood JA, Pechal JL, Krausz KL, Bose JL, Schmidt CJ, Benbow ME, Jordan HR (2016) Fluorescently labeled bacteria provide insight on post-mortem microbial transmigration. Forensic Sci Int 264:63–69. https://doi.org/10.1016/j.forsciint.2016.03.019

    Article  CAS  Google Scholar 

  • Can I, Javan GT, Pozhitkov AE, Noble PA (2014) Distinctive thanatomicrobiome signatures found in the blood and internal organs of humans. J Microbiol Methods 106:1–7. https://doi.org/10.1016/j.mimet.2014.07.026

    Article  CAS  Google Scholar 

  • Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67:1716–1725. https://doi.org/10.1136/gutjnl-2018-316723

    Article  CAS  Google Scholar 

  • Canny GO, McCormick BA (2008) Bacteria in the intestine, helpful residents or enemies from within? Infect Immun 76:3360–3373. https://doi.org/10.1128/IAI.00187-08

    Article  CAS  Google Scholar 

  • Carter DO, Metcalf JL, Bibat A, Knight R (2015) Seasonal variation of postmortem microbial communities. Forensic Sci Med Pathol 11:202–207. https://doi.org/10.1007/s12024-015-9667-7

    Article  Google Scholar 

  • Carter DO, Yellowlees D, Tibbett M (2008) Temperature affects microbial decomposition of cadavers (Rattus rattus) in contrasting soils. Appl Soil Ecol 40:129–137. https://doi.org/10.1016/j.apsoil.2008.03.010

    Article  Google Scholar 

  • Carter DO, Yellowlees D, Tibbett M (2010) Moisture can be the dominant environmental parameter governing cadaver decomposition in soil. Forensic Sci Int 200:60–66. https://doi.org/10.1016/j.forsciint.2010.03.031

    Article  Google Scholar 

  • Chaban B, Links MG, Jayaprakash TP, Wagner EC, Bourque DK, Lohn Z, Albert AYK, van Schalkwyk J, Reid G, Hemmingsen SM, Hill JE, Money DM (2014) Characterization of the vaginal microbiota of healthy Canadian women through the menstrual cycle. Microbiome 2:23. https://doi.org/10.1186/2049-2618-2-23

    Article  Google Scholar 

  • Charabidze D, Gosselin M, Hedouin V (2017) Use of necrophagous insects as evidence of cadaver relocation: myth or reality? Peer J:e3506. https://doi.org/10.7717/peerj.3506

  • Chen W, Liu F, Ling Z, Tong X, Xiang C (2012) Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 7:e39743. https://doi.org/10.1371/journal.pone.0039743

    Article  CAS  Google Scholar 

  • Cobaugh KL, Schaeffer SM, DeBruyn JM (2015) Functional and structural succession of soil microbial communities below decomposing human cadavers. PLoS One 10. https://doi.org/10.1371/journal.pone.0130201

  • Cogen AL, Nizet V, Gallo RL (2008) Skin microbiota: a source of disease or defence? Brazilian J Dermatol 158:442–455. https://doi.org/10.1111/j.1365-2133.2008.08437.x

    Article  CAS  Google Scholar 

  • Damann FE, Williams DE, Layton AC (2015) Potential use of bacterial community succession in decaying human bone for estimating postmortem interval. J Forensic Sci 60:844–850. https://doi.org/10.1111/1556-4029.12744

    Article  Google Scholar 

  • Dash HR, Das S (2018) Microbial degradation of forensic samples of biological origin: potential threat to human DNA typing. Mol Biotechnol 60(2):141–153. https://doi.org/10.1007/s12033-017-0052-5

  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nat 505:559–563. https://doi.org/10.1038/nature12820

    Article  CAS  Google Scholar 

  • Davis CD (2016) The gut microbiome and its role in obesity. Nutr Today 51:167–174. https://doi.org/10.1097/NT.0000000000000167

    Article  Google Scholar 

  • DeBruyn JM, Hauther KA (2017) Postmortem succession of gut microbial communities in deceased human subjects. Peer J 5:e3437. https://doi.org/10.7717/peerj.3437

    Article  Google Scholar 

  • Deo PN, Deshmukh R (2019) Oral microbiome: unveiling the fundamentals. J Oral Maxillofacial Pathol 23:122–128. https://doi.org/10.4103/jomfp.JOMFP_304_18

    Article  Google Scholar 

  • Desmond AU, Nicholas O, Emmanuel OO (2018) Microbial forensics: forensic relevance of the individual person’s microbial signature. Int J Life Sci Scient Res 4:2037–2043. https://doi.org/10.21276/ijlssr.2018.4.5.11

    Article  Google Scholar 

  • DeVault TL, Rhodes OE Jr, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234. https://doi.org/10.1034/j.1600-0706.2003.12378.x

    Article  Google Scholar 

  • Devkota S, Chang EB (2015) Interactions between diet, bile acid metabolism, gut microbiota, and inflammatory bowel diseases. Dig Dis 33:351–356. https://doi.org/10.1159/000371687

    Article  Google Scholar 

  • Diop K, Dufour JC, Levasseur A, Fenollar F (2019) Exhaustive repertoire of human vaginal microbiota. Hum Microb J 11:100051. https://doi.org/10.1016/j.humic.2018.11.002

    Article  Google Scholar 

  • Donaldson AE, Lamont IL (2013) Biochemistry changes that occur after death: potential markers for determining post-mortem interval. PLoS One 8:e82011. https://doi.org/10.1371/journal.pone.0082011

    Article  CAS  Google Scholar 

  • Donoghue HD (2009) Human tuberculosis—an ancient disease, as elucidated by ancient microbial biomolecules. Microbes Infect 11:1156–1162. https://doi.org/10.1016/j.micinf.2009.08.008

    Article  CAS  Google Scholar 

  • Fierera N, Lauberb CL, Zhoub N, McDonaldc D, Costelloc EK, Knight R (2010) Forensic identification using skin bacterial communities. PNAS 107:6477–6481. https://doi.org/10.1073/pnas.1000162107

    Article  Google Scholar 

  • Finley SJ, Lorenco N, Mulle J, Robertson BK, Javan GT (2015) Assessment of microbial DNA extraction methods of cadaver soil samples for criminal investigations. Aust J Forensic Sci 48:265–272. https://doi.org/10.1080/00450618.2015.1063690

    Article  Google Scholar 

  • Finley SJ, Pechal JL, Benbow ME, Robertson BK, Javan GT (2016) Microbial signatures of cadaver gravesoil during decomposition. Microb Ecol 71:524–529. https://doi.org/10.1007/s00248-015-0725-1

    Article  Google Scholar 

  • Fisman D, Patrozou E, Carmeli Y, Perencevich E, Tuite AR, Mermel LA (2014) Geographical variability in the likelihood of bloodstream infections due to Gram-negative bacteria: correlation with proximity to the equator and health care expenditure. PLoS ONE 9:e114548. https://doi.org/10.1371/journal.pone.0114548

    Article  CAS  Google Scholar 

  • Fu X, Guo J, Finkelbergs D, He J, Zha L, Guo Y, Cai J (2019) Fungal succession during mammalian cadaver decomposition and potential forensic implications. Sci Rep 9. https://doi.org/10.1038/s41598-019-49361-0

  • Gao L, Xu T, Huang G, Jiang S, Gu Y, Chen F (2018) Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell 9:488–500. https://doi.org/10.1007/s13238-018-0548-1

    Article  CAS  Google Scholar 

  • Gill JR, Landi K (2011) Putrefactive rigor: apparent rigor mortis due to gas distension. Am J Forensic Med Pathol 32:242–244. https://doi.org/10.1097/PAF.0b013e3181dd17b9

    Article  Google Scholar 

  • Goff ML (2009) Early post-mortem changes and stages of decomposition in exposed cadavers. Exp Appl Acarol 49:21–36. https://doi.org/10.1007/s10493-009-9284-9

    Article  Google Scholar 

  • Golan Y (2019) Current treatment options for acute skin and skin-structure infections. Clin Infect Dis 68:S206–S212. https://doi.org/10.1093/cid/ciz004

    Article  CAS  Google Scholar 

  • Gonzalez A, Clemente JC, Shade A, Metcalf JL, Song S, Prithiviraj B, Palmer BE, Knight R (2011) Our microbial selves: what ecology can teach us. EMBO Rep 12:775–784. https://doi.org/10.1038/embor.2011.137

    Article  CAS  Google Scholar 

  • Grandi R, Capaccio P, Bidossi A, Bottagisi M, Drago L, Torretta S, Pignataro L, De Vecchia E (2019) Salivary calculi microbiota: new insights into microbial networks and pathogens reservoir. Microbes Infect 21:109–112. https://doi.org/10.1016/j.micinf.2018.10.002

    Article  Google Scholar 

  • Gray RH, Kigozi G, Serwadda D, Makumbi F, Nalugoda F, Watya S, Moulton L, Chen MZ, Sewankambo NK, Kiwanuka N, Sempijja V, Lutalo T, Kagayii J, Wabwire-Mangen F, Ridzon R, Bacon M, Wawer MJ (2008) The effects of male circumcision on female partners' genital tract symptoms and vaginal infections in a randomized trial in Rakai, Uganda. Am J Obstet Gynecol 200:42.e17. https://doi.org/10.1016/j.ajog.2008.07.069

    Article  Google Scholar 

  • Grice EA, Kong HH, Renaud G, Young AC, NISC Comparative Sequencing Program, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA (2008) A diversity profile of the human skin microbiota. Genome Res 18:1043–1050. https://doi.org/10.1101/gr.075549.107

    Article  CAS  Google Scholar 

  • Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253. https://doi.org/10.1038/nrmicro2537

    Article  CAS  Google Scholar 

  • Grice EA, Segre JA (2012) The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170. https://doi.org/10.1146/annurev-genom-090711-163814

    Article  CAS  Google Scholar 

  • Guo J, Fu X, Liao H, Hu Z, Long L, Yan W, Ding Y, Zha L, Guo Y, Yan J, Chang Y, Cai J (2016) Potential use of bacterial community succession for estimating post-mortem interval as revealed by high-throughput sequencing. Sci Rep 6:24197. https://doi.org/10.1038/srep24197

    Article  CAS  Google Scholar 

  • Haakensen M, Dobson CM, Deneer H, Ziola B (2008) Real-time PCR detection of bacteria belonging to the Firmicutes Phylum. Int J Food Microbiol 125:236–241. https://doi.org/10.1016/j.ijfoodmicro.2008.04.002

    Article  CAS  Google Scholar 

  • Hao WL, Lee YK (2004) Microflora of the gastrointestinal tract: a review. Methods Mol Biol 268:491–502. https://doi.org/10.1385/1-59259-766-1

    Article  Google Scholar 

  • Haslam TCF, Tibbett M (2009) Soils of contrasting pH affect the decomposition of buried mammalian (Ovis aries) skeletal muscle tissue. J Forensic Sci 54:900–904. https://doi.org/10.1111/j.1556-4029.2009.01070.x

    Article  CAS  Google Scholar 

  • Hau TC, Hamzah NH, Lian HH, Hamzah SPAA (2014) Decomposition process and post mortem changes: review. Sains Malaysiana 43:1873–1882

    Article  Google Scholar 

  • Hauther KA, Cobaugh KL, Jantz LM, Sparer TE, DeBruyn JM (2015) Estimating time since death from postmortem human gut microbial communities. J Forensic Sci 60:1234–1240. https://doi.org/10.1111/1556-4029.12828

    Article  Google Scholar 

  • Hayashi H, Takahashi R, Nishi T, Sakamoto M, Benno Y (2005) Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol 54:1093–1101. https://doi.org/10.1099/jmm.0.45935-0

    Article  CAS  Google Scholar 

  • Human Microbiome Project Consortium (2012) A framework for human microbiome research. Nat 486:215–221. https://doi.org/10.1038/nature11209

    Article  CAS  Google Scholar 

  • Hyde ER, Haarmann DP, Petrosino JF, Lynne AM, Bucheli SR (2014) Initial insights into bacterial succession during human decomposition. Int J Legal Med 129:661–671. https://doi.org/10.1007/s00414-014-1128-4

    Article  Google Scholar 

  • Iancu L, Carter DO, Junkins EN, Purcarea C (2015) Using bacterial and necrophagous insect dynamics for post-mortem interval estimation during cold season: novel case study in Romania. Forensic Sci Int 254:106–117. https://doi.org/10.1016/j.forsciint.2015.07.024

    Article  Google Scholar 

  • Iancu L, Dean DE, Purcarea C (2018) Temperature influence on prevailing Necrophagous diptera and bacterial taxa with forensic implications for postmortem interval estimation: a review. J Med Entomol 55:1369–1379. https://doi.org/10.1093/jme/tjy136

    Article  Google Scholar 

  • Javan GT, Finley SJ, Can I, Wilkinson JE, Hanson JD, Tarone AM (2016) Human Thanatomicrobiome succession and time since death. Sci Rep 6:29598. https://doi.org/10.1038/srep29598

    Article  CAS  Google Scholar 

  • Javan GT, Finley SJ, Smith T, Miller J, Wilkinson JE (2017) Cadaver thanatomicrobiome signatures: the ubiquitous nature of Clostridium species in human decomposition. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02096

  • Javan GT, Finley SJ, Tuomisto S, Hall A, Benbow ME, Mills D (2019) An interdisciplinary review of the thanatomicrobiome in human decomposition. Forensic Sci Med Pathol 15:75–83. https://doi.org/10.1007/s12024-018-0061-0

    Article  Google Scholar 

  • Johnson HR, Trinidad DD, Guzman S, Khan Z, Parziale JV, DeBruyn JM, Lents NH (2016) A machine learning approach for using the postmortem skin microbiome to estimate the postmortem interval. PLoS One 11:e0167370. https://doi.org/10.1371/journal.pone.0167370

    Article  CAS  Google Scholar 

  • Jordan HR, Tomberlin JK (2017) Abiotic and biotic factors regulating inter-kingdom engagement between insects and microbe activity on vertebrate remains. Insects 8:54. https://doi.org/10.3390/insects8020054

    Article  Google Scholar 

  • Joseph I, Mathew DG, Sathyan P, Vargheese G (2011) The use of insects in forensic investigations: an overview on the scope of forensic entomology. J Forensic Dent Sci 3:89–91. https://doi.org/10.4103/0975-1475.92154

    Article  Google Scholar 

  • Jovel J, Patterson J, Wang W, Hotte N, O'Keefe S, Mitchel T, Perry T, Kao D, Mason AL, Madsen KL, Wong GKS (2016) Characterization of the gut microbiome using 16S or shotgun metagenomics. Front Microbiol 7:459. https://doi.org/10.3389/fmicb.2016.00459

    Article  Google Scholar 

  • Kang S, Denman SE, Morrison M, Yu Z, Dore J, Leclerc M, McSweeney CS (2010) Dysbiosis of fecal microbiota in Crohn’s disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis 16:2034–2042. https://doi.org/10.1002/ibd.21319

    Article  Google Scholar 

  • Kashan D, Muthu N, Chaucer B, Davalos F, Bernstein M, Chendrasekhar A (2016) Uterine perforation with intra-abdominal Clostridium perfringensgas gangrene: a rare and fatal infection. J Gynecol Surg 32:182–184. https://doi.org/10.1089/gyn.2015.0115

    Article  Google Scholar 

  • KastlJr AJ, Terry NA, Wu GD, Albenberg LG (2020) The structure and function of the human small intestinal microbiota: current understanding and future directions. Cell Mol Gastroenterol Hepatol 9:33–45. https://doi.org/10.1016/j.jcmgh.2019.07.006

    Article  Google Scholar 

  • Keeney KM, Yurist-Doutsch S, Arrieta MC, Finlay BB (2014) Effects of antibiotics on human microbiota and subsequent disease. Annu Rev Microbiol 68:217–235. https://doi.org/10.1146/annurev-micro-091313-103456

    Article  CAS  Google Scholar 

  • Khan R, Petersen FC, Shekhar S (2019) Commensal bacteria: an emerging player in defense against respiratory pathogens. Front Immunol 10:1203. https://doi.org/10.3389/fimmu.2019.01203

    Article  CAS  Google Scholar 

  • Kho ZY, Lal SK (2018) The human gut microbiome—a potential controller of wellness and disease. Front Microbiol 14. https://doi.org/10.3389/fmicb.2018.01835

  • Khosravi Y, Dieye Y, Poh BH, Ng CG, Loke MF, Goh KL, Vadivelu J (2014) Culturable bacterial microbiota of the stomach of Helicobacter pyloripositive and negative gastric disease patients. Sci World J 610421:1–10. https://doi.org/10.1155/2014/610421

    Article  CAS  Google Scholar 

  • King AJ, Freeman KR, McCormick KF, Lynch RC, Lozupone C, Knight R, Schmidt SK (2010) Biogeography and habitat modelling of high-alpinebacteria. Nat Commun 1:53. https://doi.org/10.1038/ncomms1055

    Article  CAS  Google Scholar 

  • Klaschik S, Lehmann LE, Raadts A, Book M, Hoeft A, Stuber F (2002) Real-time PCR for detection and differentiation of Gram-positive and Gram-negative bacteria. J Clin Microbiol 40:4304–4307. https://doi.org/10.1128/JCM.40.11.4304-4307.2002

    Article  CAS  Google Scholar 

  • Krajmalnik-Brown R, Ilhan ZE, Kang DW, DiBaise JK (2012) Effects of gut microbes on nutrient absorption and energy regulation. Nutr Clin Pract 27:201–214. https://doi.org/10.1177/0884533611436116

    Article  Google Scholar 

  • Langdon A, Crook N, Dantas G (2016) The effects of antibiotics on themicrobiome throughout development and alternative approaches for therapeutic modulation. Genom Med 8:39. https://doi.org/10.1186/s13073-016-0294-z

    Article  CAS  Google Scholar 

  • Lawrence KE, Lam KC, Morgun A, Shulzhenko N, Löhr CV (2019) Effect of temperature and time on the thanatomicrobiome of the cecum, ileum, kidney, and lung of domestic rabbits. J Veterin Diagno Invest 31:155–163. https://doi.org/10.1177/1040638719828412

    Article  Google Scholar 

  • Lax S, Hampton-Marcell JT, Gibbons SM, Colares GB, Smith D, Eisen JA, Gilbert JA (2015) Forensic analysis of the microbiome of phones and shoes. Microbiom 3:21. https://doi.org/10.1186/s40168-015-0082-9

    Article  Google Scholar 

  • Lee Goff M (2009) Early post-mortem changes and stages of decomposition in exposed cadavers. Exp Appl Acarol 49:21–36. https://doi.org/10.1007/s10493-009-9284-9

    Article  CAS  Google Scholar 

  • Liszt K, Zwielehner J, Handschur M, Hippe B, Thaler R, Haslberger AG (2009) Characterization of bacteria, clostridia and Bacteroides in faeces of vegetarians using qPCR and PCR-DGGE fingerprinting. Ann Nutr Metab 54:253–257. https://doi.org/10.1159/000229505

    Article  CAS  Google Scholar 

  • Lutz H, Vangelatos A, Gottel N, Speed E, Osculati A, Visona S, Finley SJ, Tuomisto S, Karhunen P, Gilbert JA, Javan GT (2019) Manner of death and demographic effects on microbial community composition in organs of the human cadaver. BioRxiv. https://doi.org/10.1101/752576

  • Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, Brochado AR, Fernandez KC, Dose H, Mori H, Patil KR, Bork P, Typas A (2018) Extensive impact of non-antibiotic drugs on human gut bacteria. Nat 555:623–628. https://doi.org/10.1038/nature25979

    Article  CAS  Google Scholar 

  • Manson JM, Rauch M, Gilmore MS (2008) The Commensal Microbiology of the Gastrointestinal Tract. In: Huffnagle GB, Noverr MC (eds) GI microbiota and regulation of the immune system, Adv Exp Med Biol, vol 635. Springer, New York

    Chapter  Google Scholar 

  • Martin DH (2012) The microbiota of the vagina and its influence on women’s health and disease. Am J Med Sci 343:2–9. https://doi.org/10.1097/MAJ.0b013e31823ea228

    Article  Google Scholar 

  • Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68:5445–5451. https://doi.org/10.1128/aem.68.11.5445-5451.2002

    Article  CAS  Google Scholar 

  • Maughan RJ, Otani H, Watson P (2012) Influence of relative humidity on prolonged exercise capacity in a warm environment. Eur J Appl Physiol 112:2313–2321. https://doi.org/10.1007/s00421-011-2206-7

    Article  Google Scholar 

  • McInnes P, Cutting M (2010) Core microbiome sampling protocol: a manual of protocols for the human microbiome project. HMP Protocol # 07-001; http://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/GetPdf.cgi?id=phd002854.2.

  • Melis C, Selva N, Teurlings I, Skarpe C, Linnell JDC, Andersen R (2007) Soil and vegetation nutrient response to bison carcasses in Białowieża Primeval Forest, Poland. Ecol Res 22:807–813. https://doi.org/10.1007/s11284-006-0321-4

    Article  CAS  Google Scholar 

  • Metcalf JL, Carter DO, Knight R (2016a) Microbiology of death. Curr Biol 26:R543–R576. https://doi.org/10.1016/j.cub.2016.03.042

    Article  CAS  Google Scholar 

  • Metcalf JL, Xu ZZ, Weiss S, Lax S, Treuren WV, Hyde ER, Song SJ, Amir A, Larsen P, Sangwan N, Haarmann D, Humphrey GC, Ackermann G, Thompson LR, Lauber C, Bibat A, Nicholas C, Gebert MJ, Petrosino JF, Reed SC, Gilbert JA, Lynne AM, Bucheli SR, Carter DO, Knight R (2016b) Microbial community assembly and metabolic function during mammalian corpse decomposition. Sci 351:158–162. https://doi.org/10.1126/science.aad2646

    Article  CAS  Google Scholar 

  • Meyer J, Anderson B, Carter DO (2013) Seasonal variation of carcass decomposition and grave soil chemistry in a cold (Dfa) climate. J Forensic Sci 58:1175–1182. https://doi.org/10.1111/1556-4029.12169

    Article  Google Scholar 

  • Morris JA, Harrison LM, Partridge SM (2006) Postmortem bacteriology: a re-evaluation. J Clin Pathol 59:1–9. https://doi.org/10.1136/jcp.2005.028183

    Article  CAS  Google Scholar 

  • Muhamed AMC, Atkins K, Stannard SR, Mündel T, Thompson MW (2016) The effects of a systematic increase in relative humidity on thermoregulatory and circulatory responses during prolonged running exercise in the heat. Temperature 3:455–464. https://doi.org/10.1080/23328940.2016.1182669

    Article  Google Scholar 

  • Nava GM, Stappenbeck TS (2011) Diversity of the autochthonous colonic microbiota. Gut Microbes 2:9–104. https://doi.org/10.4161/gmic.2.2.15416

    Article  Google Scholar 

  • Ngaihte P, Zomawia E, Kaushik I (2019) Cancer in the NorthEast India: where we are and what needs to be done? Indian J Public Health 63:251–253. https://doi.org/10.4103/ijph.IJPH_323_18

    Article  Google Scholar 

  • Nogueira T, David PHC, Pothier J (2019) Antibiotics as both friends and foes of the human gut microbiome: the microbial community approach. Drug Dev Res 80:86–97. https://doi.org/10.1002/ddr.21466

    Article  CAS  Google Scholar 

  • Oh J, Byrd AL, Park M, Kong HH, Segre JA (2016) Temporal stability of the human skin microbiome. Cell 165:854–866. https://doi.org/10.1016/j.cell.2016.04.008

    Article  CAS  Google Scholar 

  • Onderdonk AB, Delaney ML, Fichorova RN (2016) The human microbiome during bacterial vaginosis. Clin Microbiol Rev 29:223–238. https://doi.org/10.1128/CMR.00075-15

    Article  CAS  Google Scholar 

  • Panizzon JP, Júnior HLP, Knaak N, Ramos RC, Ziegler DR, Fiuza LM (2015) Microbial diversity: relevance and relationship between environmental conservation and human health. Braz Arch Biol Technol 58:137–145. https://doi.org/10.1590/S1516-8913201502821

    Article  Google Scholar 

  • Patel K, Clifford DB (2014) Bacterial brain abscess. Neurohospitalist 4:196–204. https://doi.org/10.1177/1941874414540684

    Article  Google Scholar 

  • Payne JA (1965) A summer carrion study of the baby pig Sus Scrofa Linnaeus. Ecol 46:592–602

    Article  Google Scholar 

  • Pechal JL, Crippen TL, Benbow ME, Tarone AM, Dowd S, Tomberlin JK (2014) The potential use of bacterial community succession in forensics as described by high throughput metagenomic sequencing. Int J Legal Med 128:193–205. https://doi.org/10.1007/s00414-013-0872-1

    Article  Google Scholar 

  • Pechal JL, Crippen TL, Tarone AM, Lewis AJ, Tomberlin JK, Benbow ME (2013) Microbial community functional change during vertebrate carrion decomposition. PLoS One 8:e79035. https://doi.org/10.1371/journal.pone.0079035

    Article  CAS  Google Scholar 

  • Price LB, Liu CM, Johnson KE, Aziz M, Lau MK, Bowers J, Ravel J, Keim PS, Serwadda D, Wawer MJ, Gray RH (2010) The effects of circumcision on the penis microbiome. PLoS One 5:e8422. https://doi.org/10.1371/journal.pone.0008422

    Article  CAS  Google Scholar 

  • Purkayastha SD, Bhattacharya MK, Prasad HK, Upadhyaya H, Lala SD, Pal K, Das M, Sharma GD, Bhattacharjee MJ (2019) Contrasting diversity of vaginal lactobacilli among the females of Northeast India. BMC Microbiol 19:198. https://doi.org/10.1186/s12866-019-1568-6

    Article  Google Scholar 

  • Ramakrishna BS (2007) The normal bacterial flora of the human intestine and its regulation. J Clin Gastroenterol 41:S2–S6. https://doi.org/10.1097/MCG.0b013e31802fba68

    Article  Google Scholar 

  • Reller LB, Weinstein MP, Procop GW, Wilson M (2001) Infectious disease pathology. Clin Infect Dis 32:1589–1601. https://doi.org/10.1086/320537

    Article  Google Scholar 

  • Ribet D, Cossart P (2015) How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 17:173–183. https://doi.org/10.1016/j.micinf.2015.01.004

    Article  CAS  Google Scholar 

  • Riedel S (2014) The value of postmortem microbiology cultures. J Clin Microbiol 52:1028–1033. https://doi.org/10.1128/JCM.03102-13

    Article  Google Scholar 

  • Rivers D, Geiman T (2017) Insect artifacts are more than just altered blood stains. Insects 8:37. https://doi.org/10.3390/insects8020037

    Article  Google Scholar 

  • Robertson RC, Manges AR, Finlay BB, Prendergast AJ (2019) The human microbiome and child growth—first 1000 days and beyond. Trends Microbiol 27:131–147. https://doi.org/10.1016/j.tim.2018.09.008

    Article  CAS  Google Scholar 

  • Salama NR, Hartung ML, Müller A (2013) Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 11:385–399. https://doi.org/10.1038/nrmicro3016

    Article  CAS  Google Scholar 

  • Sanford MR (2017) Insects and associated arthropods analyzed during medicolegal death investigations in Harris County, Texas, USA: January 2013- April 2016. PLoS One 12:e0179404. https://doi.org/10.1371/journal.pone.0179404

    Article  CAS  Google Scholar 

  • Sansonetti PJ (2011) To be or not to be a pathogen: that is the mucosally relevant question. Mucosal Immunol 4:8–14. https://doi.org/10.1038/mi.2010.77

    Article  CAS  Google Scholar 

  • Saraswat PK, Nirwan PS, Saraswat S, Mathur P (2008) Biodegradation of dead bodies including human cadavers and their safe disposal with reference to mortuary practice. J Indian Acad Forensic Med 30:273–280

    Google Scholar 

  • Schmedes SE, Woerner AE, Budowle B (2017) Forensic human identification using skin microbiomes. Appl Environ Microbiol 83:e01672–e01617. https://doi.org/10.1128/AEM.01672-17

    Article  CAS  Google Scholar 

  • Schubert AM, Rogers MA, Ring C, Mogle J, Petrosino JP, Young VB, Aronoff DM, Schloss PD (2014) Microbiome data distinguish patients with Clostridium difficile infection and non-C. difficile associated diarrhea from healthy controls. mBio 5:e01021–e01014. https://doi.org/10.1128/mBio.01021-14

    Article  CAS  Google Scholar 

  • Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14(8):e1002533. https://doi.org/10.1371/journal.pbio.1002533

    Article  CAS  Google Scholar 

  • Sharma A, Kawarabayasi Y, Satyanarayana T (2012) Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16:1–19. https://doi.org/10.1007/s00792-011-0402-3

    Article  CAS  Google Scholar 

  • Sharma R, Garg RK, Gaur JR (2015) Various methods for the estimation of the post mortem interval from Calliphoridae: a review. Egypt J Forensic Sci 5:1–12. https://doi.org/10.1016/j.ejfs.2013.04.002

    Article  Google Scholar 

  • Shedge R, Krishan K, Warrier V, Kanchan T (2019) Postmortem changes. In: StatPearls [Internet]. StatPearls Publishing, Treasure Island (FL) 2020 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK539741/

    Google Scholar 

  • Singh B, Minick KJ, Strickland MS, Wickings KG, Crippen TL, Tarone AM, Benbow ME, Sufrin N, Tomberlin JK, Pechal JL (2018) Temporal and spatial impact of human cadaver decomposition on soil bacterial and arthropod community structure and function. Front Microbiol 8:2616. https://doi.org/10.3389/fmicb.2017.02616

    Article  Google Scholar 

  • Stearns JC, Lynch MDJ, Senadheera DB, Tenenbaum HC, Goldberg MB, Cvitkovitch DG, Croitoru K, Hagelsieb GM, Neufeld JD (2011) Bacterial biogeography of the human digestive tract. Sci Rep 170:2011. https://doi.org/10.1038/srep00170

    Article  CAS  Google Scholar 

  • Sulyanto RM, Thompson ZA, Beall CJ, Leys EJ, Griffen AL (2019) The predominant oral microbiota is acquired early in an organized pattern. Sci Rep 9:10550. https://doi.org/10.1038/s41598-019-46923-0

    Article  CAS  Google Scholar 

  • Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, LoeningBaucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H (2002) Mucosal flora in inflammatory bowel disease. Gastroenterol 122:44–54. https://doi.org/10.1053/gast.2002.30294

    Article  Google Scholar 

  • Thomas TB, Finley SJ, Wilkinson JE, Wescott DJ, Gorski A, Javan GT (2017) Postmortem microbial communities in burial soil layers of skeletonized humans. J Forensic Legal Med 49:43–49. https://doi.org/10.1016/j.jflm.2017.05.009

    Article  Google Scholar 

  • Thursby E, Juge N (2017) Introduction to the human gut microbiota. Biochem J 474:1823–1836. https://doi.org/10.1042/BCJ20160510

    Article  CAS  Google Scholar 

  • Tomberlin JK, Mohr R, Benbow ME, Tarone AM, VanLaerhoven S (2011) A roadmap for bridging basic and applied research in forensic entomology. Annu Rev Entomol 56:401–421. https://doi.org/10.1146/annurev-ento-051710-103143

    Article  CAS  Google Scholar 

  • Tu Q, He Z, Zhou J (2014) Strain/species identification in metagenomes using genome-specific markers. Nucleic Acids Res 42:e67. https://doi.org/10.1093/nar/gku138

    Article  CAS  Google Scholar 

  • Tu Q, Li J, Shi Z, Chen Y, Lin L, Li J, Wang H, Yan J, Zhou Q, Li X, Li L, Zhou J, He Z (2017) HuMiChip2 for strain level identification and functional profiling of human microbiomes. Appl Microbiol Biotechnol 101:423–435. https://doi.org/10.1007/s00253-016-7910-0

    Article  CAS  Google Scholar 

  • Tuomisto S, Karhunen PJ, Vuento R, Aittoniemi J, Pessi T (2013) Evaluation of postmortem bacterial migration using culturing and real-time quantitative PCR. J Forensic Sci 58:910–916. https://doi.org/10.1111/1556-4029.12124

    Article  CAS  Google Scholar 

  • Ursell LK, Metcalf JL, Parfrey LW, Knight R (2012) Defining the human microbiome. Nutr Rev 70:S38–S44. https://doi.org/10.1111/j.1753-4887.2012.00493.x

    Article  Google Scholar 

  • Vass AA, Barshick SA, Sega G, Caton J, Skeen JT, Love JC, Synstelien JA (2002) Decomposition chemistry of human remains: a new methodology for determining the postmortem interval. J Forensic Sci 47:542–553

  • Vila AV, Collij V, Sanna S, Sinha T, Imhann F, Bourgonje AR, Mujagic Z, Jonkers DMAE, Masclee AAM, Fu J, Kurilshikov A, Wijmenga C, Zhernakova A, Weersma RK (2020) Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat Commun 11:362. https://doi.org/10.1038/s41467-019-14177-z

    Article  CAS  Google Scholar 

  • Vinay J, Harish S, Mangala GSR, Hugar BS (2017) A study on postmortem wound dating by gross and histopathological examination of abrasions. Am J Forensic Med Pathol 38:167–173. https://doi.org/10.1097/PAF.0000000000000314

    Article  Google Scholar 

  • Wang B, Yao M, Lv L, Ling Z, Li L (2017) The human microbiota in health and disease. Engin 3:71–82. https://doi.org/10.1016/J.ENG.2017.01.008

    Article  Google Scholar 

  • Wang D, He N, Wang Q, Lu Y, Wang Q, Xu Z, Zhu J (2016) Effects of temperature and moisture on soil organic matter decomposition along elevation gradients on the Changbai mountains, northeast china. Pedosphere (online) 26:399–407. https://doi.org/10.1016/S1002-0160(15)60052-2

    Article  Google Scholar 

  • Wang H, Wei CX, Min L, Zhu LY (2018) Good or bad: gut bacteria in human health and diseases. Biotechnol Biotechnol Equip 32:1075–1080. https://doi.org/10.1080/13102818.2018.1481350

    Article  CAS  Google Scholar 

  • Weiss S, Carter DO, Metcalf JL, Knight R (2016) Carcass mass has little influence on the structure of grave soil microbial communities. Int J Legal Med 130:253–263. https://doi.org/10.1007/s00414-015-1206-2

    Article  Google Scholar 

  • Williams T, Soni S, White J, Can G, Javan GT (2015) Evaluation of DNA degradation using flow cytometry: promising tool for postmortem interval determination. Forensic Med Pathol 36:104–110. https://doi.org/10.1097/PAF.0000000000000146

    Article  Google Scholar 

  • Yang YW, Chen MK, Yang BY, Huang XJ, Zhang XR, He LQ, Zhang J, Hua ZC (2015) Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in mouse feces. Appl Environ Microbiol 81:6749–6756. https://doi.org/10.1128/AEM.01906-15

    Article  CAS  Google Scholar 

  • Yeoh YK, Chan MH, Chen Z, Lam EWH, Wong PY, Ngai CM, Chan PKS, Hui M (2019) The human oral cavity microbiota composition during acute tonsillitis: a cross-sectional survey. BMC Oral Health 19:275. https://doi.org/10.1186/s12903-019-0956-5

    Article  Google Scholar 

  • Zhou C, Byard RW (2011) Factors and processes causing accelerated decomposition in human cadavers—an overview. J Forensic Legal Med 18:6–9. https://doi.org/10.1016/j.jflm.2010.10.003

    Article  Google Scholar 

  • Zhou W, Bian Y (2018) Thanatomicrobiome composition profiling as a tool for forensic investigation. Forensic Sci Res 3:105–110. https://doi.org/10.1080/20961790.2018.1466430

    Article  Google Scholar 

  • Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CGM, Troost FJ, Bork P, Wels M, de Vos WM, Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6:1415–1426. https://doi.org/10.1038/ismej.2011.212

    Article  CAS  Google Scholar 

  • Zolfo M, Asnicar F, Manghi P, Pasolli E, Tett A, Segata N (2018) Profiling microbial strains in urban environments using metagenomic sequencing data. Biol Direct 13:9. https://doi.org/10.1186/s13062-018-0211-z

    Article  CAS  Google Scholar 

  • Zozaya M, Ferris MJ, Siren JD, Lillis R, Myers L, Nsuami MJ, Eren AM, Brown J, Taylor CM, Martin DH (2016) Bacterial communities in penile skin, male urethra, and vaginas of heterosexual couples with and without bacterial vaginosis. Mirobiome 4:16. https://doi.org/10.1186/s40168-016-0161-6

    Article  Google Scholar