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Microbial Signatures of Cadaver Gravesoil During Decomposition

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Abstract

Genomic studies have estimated there are approximately 103–106 bacterial species per gram of soil. The microbial species found in soil associated with decomposing human remains (gravesoil) have been investigated and recognized as potential molecular determinants for estimates of time since death. The nascent era of high-throughput amplicon sequencing of the conserved 16S ribosomal RNA (rRNA) gene region of gravesoil microbes is allowing research to expand beyond more subjective empirical methods used in forensic microbiology. The goal of the present study was to evaluate microbial communities and identify taxonomic signatures associated with the gravesoil human cadavers. Using 16S rRNA gene amplicon-based sequencing, soil microbial communities were surveyed from 18 cadavers placed on the surface or buried that were allowed to decompose over a range of decomposition time periods (3–303 days). Surface soil microbial communities showed a decreasing trend in taxon richness, diversity, and evenness over decomposition, while buried cadaver-soil microbial communities demonstrated increasing taxon richness, consistent diversity, and decreasing evenness. The results show that ubiquitous Proteobacteria was confirmed as the most abundant phylum in all gravesoil samples. Surface cadaver-soil communities demonstrated a decrease in Acidobacteria and an increase in Firmicutes relative abundance over decomposition, while buried soil communities were consistent in their community composition throughout decomposition. Better understanding of microbial community structure and its shifts over time may be important for advancing general knowledge of decomposition soil ecology and its potential use during forensic investigations.

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References

  1. Vass AA (2001) Beyond the grave-understanding human decomposition. Microbiol Today 28:190–192

    Google Scholar 

  2. Hyde ER, Haarmann DP, Lynne AM, Bucheli SR, Petrosino JF (2013) The living dead: bacterial community structure of a cadaver at the onset and end of the bloat stage of decomposition. PLoS One 8, e77733. doi:10.1371/journal.pone.0077733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hyde ER, Haarmann DP, Petrosino JF, Lynne AM, Bucheli SR (2015) Initial insights into bacterial succession during human decomposition. Int J Legal Med 129:661–671

    Article  PubMed  Google Scholar 

  4. 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. doi:10.1111/1556-4029.12828

    Article  PubMed  Google Scholar 

  5. Gans J, Woilinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390

    Article  CAS  PubMed  Google Scholar 

  6. Metcalf JL, Wegener Parfrey L, Gonzalez A, Lauber CL, Knights D, Ackermann G, Humphrey GC, Gebert MJ, Van Treuren W, Berg-Lyons D, Keepers K, Guo Y, Bullard J, Fierer N, Carter DO, Knight R (2013) A microbial clock provides an accurate estimate of the postmortem interal in a mouse model system. ELife 2, e01104. doi:10.7554/eLife.01104

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lauber CL, Metcalf JL, Keepers K, Ackermann G, Carter DO, Knight R (2014) Vertebrate decomposition is accelerated by soil microbes. Appl Environ Microbiol 80:4920–4929. doi:10.1128/AEM.00957-14

    Article  PubMed  PubMed Central  Google Scholar 

  8. Weiss, S, Carter DO, Metcalf JL, Knight R (2015) Carcass mass has little influence on the structure of gravesoil microbial communities. Int J Legal Med (in press). doi:10.1007/s00414-015-1206-2

  9. Payne J (1965) A summer carrion study of the baby pig Sus Scrofa Linnaeus. Ecology 46:592–602. doi:10.2307/1934999

    Article  Google Scholar 

  10. 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. doi:10.1007/s00414-013-0872-1

    Article  PubMed  Google Scholar 

  11. Pechal JL, Benbow ME, Crippen TL, Tarone AM, Tomberlin JK (2014) Delayed insect access alters carrion decomposition and necrophagous insect community assembly. Ecosphere 5:art45

    Article  Google Scholar 

  12. Carter DO, Yellowlees D, Tibbett M (2007) Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften 94:12–24. doi:10.1007/s00114-006-0159-1

    Article  CAS  PubMed  Google Scholar 

  13. Carter DO, Metcalf JL, Bibat A, Knight R (2015) Seasonal variation of postmortem microbial communities. Forensic Sci Med Pathol 11:202–227. doi:10.1007/s12024-015-9667-7

    Article  PubMed  Google Scholar 

  14. 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 (in press). doi:10.1111/1556-4029.12859

  15. Benbow ME, Lewis AJ, Tomberlin JK, Pechal JL (2013) Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. J Med Entomol 50:440–450. doi:10.1603/ME12194

    Article  CAS  PubMed  Google Scholar 

  16. 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. doi:10.1146/annurev-ento-051710-103143

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  18. Metcalf JL, Xu ZZ, Weiss S, Lax S, Van Treuren W, Hyde ER, et al. (2015). Microbial community assembly and metabolic function during mammalian corpse decomposition. Science aad2646

  19. Cobaugh KL, Schaeffer SM, DeBruyn JM (2015) Functional and structural succession of soil microbial communities below decomposing human cadavers. PLoS ONE 10, e0130201. doi:10.1371/journal.pone.0130201

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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. doi:10.1016/j.mimet.2014.07.026

    Article  CAS  PubMed  Google Scholar 

  21. Maujean G, Guinet T, Fanton L, Malicier D (2013) The interest of postmortem bacteriology in putrefied bodies. J Forensic Sci 58:1069–1070. doi:10.1111/1556-4029.12155

    Article  PubMed  Google Scholar 

  22. Moreno LI, Mills D, Fetscher J, John-Williams K, Meadows-Jantz L, McCord B (2011) The application of amplicon length heterogeneity PCR (LH-PCR) for monitoring the dynamics of soil microbial communities associated with cadaver decomposition. J Microbiol Methods 84:388–393. doi:10.1016/j.mimet.2010.11.023

    Article  CAS  PubMed  Google Scholar 

  23. 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. doi:10.1371/journal.pone.0079035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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. doi:10.1111/1556-4029.12124

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  26. Forbes SL, Perrault KA (2014) Decomposition odour profiling in the air and soil surrounding vertebrate carrion. PLoS ONE 9, e95107. doi:10.1371/journal.pone.0095107

    Article  PubMed  PubMed Central  Google Scholar 

  27. Barnes PW, Liang SY, Jessup KE, Ruiseco LE, Phillips PL, Reagan SJ (2000) Soils, topography and vegetation of the Freeman Ranch, Freeman Ranch publication series no. 1. Southwest Texas State University Press, San Marcos

    Google Scholar 

  28. Carson D (2000) Soils of the Freeman Ranch, Hays County, Texas. Freeman Ranch publication series no. 4-2000. Southwest Texas State University Press, San Marcos

    Google Scholar 

  29. Heilman JL, McInnes KJ, Kjelgaard JF, Owens MK, Schwinning S (2007) Energy balance and water use in a subtropical karst woodland on the Edwards Plateau, Texas. J Hydrol 373:426–435

    Article  Google Scholar 

  30. 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 1–8. doi:10.1080/00450618.2015.1063690

  31. Wallenius K, Rita H, Simpanen S, Mikkonen A, Niemi RM (2010) Sample storage for soil enzyme activity and bacterial community profiles. J Microbiol Methods 81:48–55. doi:10.1016/j.mimet.2010.01.021

    Article  CAS  PubMed  Google Scholar 

  32. Caporaso JG, Knight R, Kelley ST (2011) Host-associated and free-living phage communities differ profoundly in phylogenetic composition. PLoS ONE 6, e16900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Claesson MJ, Wang Q, O’Sullivan O, Greene-Diniz R, Cole JR, Ross RP et al (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 38, e200

    Article  PubMed  PubMed Central  Google Scholar 

  36. Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman F, Costello E et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. doi:10.1038/nmeth.2276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  40. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, et al (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290. doi:10.1038/ismej.2007.53

  41. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

  42. Gunn A, Pitt SJ (2012) Microbes as forensic indicators. Trop Biomed 29:311–330

    Google Scholar 

  43. Mann RW, Bass WM, Meadows L (1990) Time since death and decomposition of the human body: variables and observations in case and experimental field studies. J Forensic Sci 35:103–111

    CAS  PubMed  Google Scholar 

  44. Vass AA, Bass WM, Wolt JD, Foss JE, Ammons JT (1992) Time since death determinations of human cadavers using soil solution. J Forensic Sci 37:1236–1253

    Article  CAS  PubMed  Google Scholar 

  45. Vass AA (2011) The elusive universal post-mortem interval formula. Forensic Sci Int 204:34–40

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Daniel J. Wescott and Sophia R. Mavroudas of the FARF at Texas State University for use of their facilities and support from their staff. We also thank the donors to the FARF whose generous gifts make this type of research feasible. Many thanks are extended to Vida Dennis for the very helpful comments during the preparation of this manuscript. This work was supported by the National Science Foundation (NSF) grants HRD 1401075, 1432991, 1433004 and discretionary funds of Michigan State University to MEB.

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    Authors and Affiliations

    1. Ph.D. Program in Microbiology, Department of Biological Sciences, Alabama State University, Montgomery, AL, 36104, USA

      Sheree J. Finley & B. K. Robertson

    2. Department of Entomology, Michigan State University, East Lansing, MI, 48824, USA

      Jennifer L. Pechal & M. Eric Benbow

    3. Department of Osteopathic Medical Specialties, Michigan State University, East Lansing, MI, 48824, USA

      M. Eric Benbow

    4. Forensic Science Program, Physical Sciences Department, Alabama State University, 915 S. Jackson St., Hatch Hall Building Room 251, Montgomery, AL, 36104, USA

      Gulnaz T. Javan

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    1. Sheree J. Finley
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    Correspondence to Gulnaz T. Javan.

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    Sheree J. Finley and Jennifer L. Pechal contributed equally to this work.

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    Finley, S.J., Pechal, J.L., Benbow, M.E. et al. Microbial Signatures of Cadaver Gravesoil During Decomposition. Microb Ecol 71, 524–529 (2016). https://doi.org/10.1007/s00248-015-0725-1

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