Metatranscriptomics: an approach for retrieving novel eukaryotic genes from polluted and related environments

Mukherjee, Arkadeep; Reddy, M. Sudhakara

doi:10.1007/s13205-020-2057-1

Review Article
Published: 27 January 2020

Metatranscriptomics: an approach for retrieving novel eukaryotic genes from polluted and related environments

3 Biotech volume 10, Article number: 71 (2020) Cite this article

1159 Accesses
10 Citations
3 Altmetric
Metrics details

Abstract

Metatranscriptomics, a subset of metagenomics, provides valuable information about the whole gene expression profiling of complex microbial communities of an ecosystem. Metagenomic studies mainly focus on the genomic content and identification of microbes present within a community, while metatranscriptomics provides the diversity of the active genes within such community, their expression profile and how these levels change due to change in environmental conditions. Metatranscriptomics has been applied to different types of environments, from the study of human microbiomes, to those found in plants, animals, within soils and in aquatic systems. Metatranscriptomics, based on the utilization of mRNA isolated from environmental samples, is a suitable approach to mine the eukaryotic gene pool for genes of biotechnological relevance. Also, it is imperative to develop different bioinformatic pipelines to analyse the data obtained from metatranscriptomic analysis. In the present review, we summarise the metatranscriptomics applied to soil environments to study the functional diversity, and discuss approaches for isolating the genes involved in organic matter degradation and providing tolerance to toxic metals, role of metatranscriptomics in microbiome research, various bioinformatics pipelines used in data analysis and technical challenges for gaining biologically meaningful insight of this approach.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Abubucker S, Segata N, Gol J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8:e1002358. https://doi.org/10.1371/journal.pcbi.1002358
CAS Article PubMed PubMed Central Google Scholar
Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105(Supplement 1):11512–11519. https://doi.org/10.1073/pnas.0801925105
Article PubMed Google Scholar
Azizan MS, Zamani AI, Stahmann KP, Ng CL (2016) Fungal metabolites and their industrial importance: a brief review. Malays J Biochem Mol Biol 19:15–23
Google Scholar
Bailly J, Fraissinet-Tachet L, Verner MC, Debaud JC, Lemaire M, Wésolowski-Louvel MR (2007) Soil eukaryotic functional diversity, a metatranscriptomic approach. ISME J 17:632–642. https://doi.org/10.1038/ismej.2007.68
CAS Article Google Scholar
Bashiardes S, Zilberman-Schapira G, Elinav E (2016) Use of metatranscriptomics in microbiome research. Bioinform Biol insights. https://doi.org/10.4137/BBI.S34610
Article PubMed PubMed Central Google Scholar
Bending GD, Rodriguez-Cruz MS, Lincoln SD (2007) Fungicide impacts on microbial communities in soils with contrasting management histories. Chemosphere 69:82–88. https://doi.org/10.1016/j.chemosphere.2007.04.042
CAS Article PubMed Google Scholar
Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci USA 105:10583–10588. https://doi.org/10.1073/pnas.0709942105
Article PubMed Google Scholar
Binz PA, Kägi JHR (1999) Metallothionein: molecular evolution and classification. In: Klaassen CD (ed) Metallothionein IV. Advances in life sciences. Birkhäuser, Basel, pp 7–13
Google Scholar
Blindauer CA (2013) Lessons on the critical interplay between zinc binding and protein structure and dynamics. J Inorg Biochem 121:145–155. https://doi.org/10.1016/j.jinorgbio.2013.01.005
CAS Article PubMed Google Scholar
Boekel J, Chilton JM, Cooke IR, Horvatovich PL, Jagtap PD, Käll L, Lehtiö J, Lukasse P, Moerland PD, Griffin TJ (2015) Multi-omic data analysis using Galaxy. Nat Biotechnol 33:137–139. https://doi.org/10.1038/nbt.3134
CAS Article PubMed Google Scholar
Botero LM, D’imperio S, Burr M, McDermott TR, Young M, Hassett DJ (2005) Poly (A) polymerase modification and reverse transcriptase PCR amplification of environmental RNA. Appl Environ Microbiol 71:1267–1275. https://doi.org/10.1128/AEM.71.3.1267-1275.2005
CAS Article PubMed PubMed Central Google Scholar
Bragalini C, Ribiere C, Parisot N, Vallon L, Prudent E, Peyretaillade E, Girlanda M, Peyret P, Marmeisse R, Luis P (2014) Solution hybrid selection capture for the recovery of functional full-length eukaryotic cDNAs from complex environmental samples. DNA Res. 21:685–694. https://doi.org/10.1093/dnares/dsu030
CAS Article PubMed PubMed Central Google Scholar
Brim H, Heyndrickx M, De Vos P, Wilmotte A, Springael D, Schlegel HG, Mergeay M (1999) Amplified rDNA restriction analysis and further genotypic characterisation of metal-resistant soil bacteria and related facultative hydrogenotrophs. Syst Appl Microbiol 22:258–268. https://doi.org/10.1016/S0723-2020(99)80073-3
CAS Article PubMed Google Scholar
Capdevila M, Atrian S (2011) Metallothionein protein evolution: a miniassay. J Biol Inorg Chem 16:977–989. https://doi.org/10.1007/s00775-011-0798-3
CAS Article PubMed Google Scholar
Carvalhais LC, Dennis PG, Tyson GW, Schenk PM (2012) Application of metatranscriptomics to soil environments. J Microbiol Meth 91:246–251. https://doi.org/10.1016/j.mimet.2012.08.011
CAS Article Google Scholar
Cervantes C, Gutierrez-Corona F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137. https://doi.org/10.1111/j.1574-6976.1994.tb00083.x
CAS Article PubMed Google Scholar
Chao-Rong GE, Zhang QC (2011) Microbial community structure and enzyme activities in a sequence of copper-polluted soils. Pedosphere 21:164–169. https://doi.org/10.1016/S1002-0160(11)60114-8
Article Google Scholar
Chenchik A, Zhu YY, Diatchenko L, Li R, Hill J, Siebert PD (1998) Generation and use of high-quality cDNA from small amounts of total RNA by SMART PCR. In: Siebert PD, Larrick JW (eds) RT-PCR Methods for gene cloning and analysis. Eaton Publishing, Natick, MA, pp 305–319
Google Scholar
Clarke J, Wu HC, Jayasinghe L, Patel A, Reid S, Bayley H (2009) Continuous base identification for single-molecule nanopore DNA sequencing. Nat Nanotechnol 4:265–270. https://doi.org/10.1038/nnano.2009.12
CAS Article PubMed Google Scholar
Clement BG, Kehl LE, DeBord KL, Kitts CL (1998) Terminal restriction fragment patterns (TRFPs), a rapid, PCR-based method for the comparison of complex bacterial communities. J Microbiol Meth 31:135–142. https://doi.org/10.1016/S0167-7012(97)00105-X
CAS Article Google Scholar
Comtet-Marre S, Parisot N, Lepercq P, Chaucheyras-Durand F, Mosoni P, Peyretaillade E, Bayat AR, Shingfield KJ, Peyret P, Forano E (2017) Metatranscriptomics reveals the active bacterial and eukaryotic fibrolytic communities in the rumen of dairy cow fed a mixed diet. Front Microbiol 8:67. https://doi.org/10.3389/fmicb.2017.00067
Article PubMed PubMed Central Google Scholar
D’Alessio JM, Gerard GF (1988) Second-strand cDNA synthesis with E. coli DNA polymerase I and RNase H: the fate of information at the mRNA 5'terminus and the effect of E. coli DNA ligase. Nucleic Acids Res 16:1999–2014. https://doi.org/10.1093/nar/16.5.1999
Article PubMed PubMed Central Google Scholar
Dai X, Tian Y, Li J, Su X, Wang X, Zhao S, Liu L, Luo Y, Liu D, Zheng H, Wang J, Dong Z, Hu S, Huang L (2015) Metatranscriptomic analyses of plant cell wall polysaccharide degradation by microorganisms in the cow rumen. Appl Environ Microbiol 81:1375–1386. https://doi.org/10.1128/AEM.03682-14
CAS Article PubMed PubMed Central Google Scholar
Damon C, Vallon L, Zimmermann S, Haider MZ, Galeote V, Dequin S, Luis P, Fraissinet-Tachet L, Marmeisse R (2011) A novel fungal family of oligopeptide transporters identified by functional metatranscriptomics of soil eukaryotes. ISME J 5:1871–1880. https://doi.org/10.1038/ismej.2011.67
CAS Article PubMed PubMed Central Google Scholar
Damon C, Lehembre F, Oger-Desfeux C, Luis P, Ranger J, Fraissinet-Tachet L, Marmeisse R (2012) Metatranscriptomics reveals the diversity of genes expressed by eukaryotes in forest soils. PLoS ONE 7:e28967. https://doi.org/10.1371/journal.pone.0028967
CAS Article PubMed PubMed Central Google Scholar
Daniel R (2002) Construction of environmental libraries for functional screening of enzyme activity. In: Brakmann S, Johnsson K (eds) Directed molecular evolution of proteins: or how to improve enzymes for biocatalysis, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 63–78. https://doi.org/10.1002/3527600647.ch4
Daniel R (2005) The metagenomics of soil. Nat Rev Microbiol 3:470–478. https://doi.org/10.1038/nrmicro1160
CAS Article PubMed Google Scholar
Degens BP, Schipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33:1143–1153. https://doi.org/10.1016/S0038-0717(01)00018-9
CAS Article Google Scholar
Dell’Amico E, Mazzocchi M, Cavalca L, Allievi L, Andreoni V (2008) Assessment of bacterial community structure in a long-term copper-polluted ex-vineyard soil. Microbiol Res 163:671–683. https://doi.org/10.1016/j.micres.2006.09.003
CAS Article PubMed Google Scholar
Deng W, Xi D, Mao H, Wanapat M (2008) The use of molecular techniques based on ribosomal RNA and DNA for rumen microbial ecosystem studies: a review. Mol Biol Rep 35:265–274. https://doi.org/10.1007/s11033-007-9079-1
CAS Article PubMed Google Scholar
Dominati E, Patterson M, Mackay A (2010) A framework for classifying and quantifying the natural capital and ecosystem services of soils. Ecol Eng 69:1858–1868. https://doi.org/10.1016/j.ecolecon.2010.05.002
Article Google Scholar
Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15:3–11. https://doi.org/10.1016/S0929-1393(00)00067-6
Article Google Scholar
Eichner CA, Erb RW, Timmis KN, Wagner-Döbler I (1999) Thermal gradient gel electrophoresis analysis of bioprotection from pollutant shocks in the activated sludge microbial community. Appl Environ Microbiol 65:102–109
CAS Article Google Scholar
Ferrer M, Martínez-Martínez M, Bargiela R, Streit WR, Golyshina OV, Golyshin PN (2016) Estimating the success of enzyme bioprospecting through metagenomics: current status and future trends. Microb Biotechnol 9:22–34. https://doi.org/10.1111/1751-7915.12309
CAS Article PubMed Google Scholar
Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S, Knight R (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microbiol 73:7059–7066. https://doi.org/10.1128/AEM.00358-07
CAS Article PubMed PubMed Central Google Scholar
Gelsomino A, Keijzer-Wolters AC, Cacco G, van Elsas JD (1999) Assessment of bacterial community structure in soil by polymerase chain reaction and denaturing gradient gel electrophoresis. J Microbiol Meth 38:1–15. https://doi.org/10.1016/S0167-7012(99)000548
CAS Article Google Scholar
Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. https://doi.org/10.1126/science.1124234
CAS Article PubMed PubMed Central Google Scholar
Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414. https://doi.org/10.1016/S0038-0717(97)00270-8
CAS Article Google Scholar
Goldmann K, Schöning I, Buscot F, Wubet T (2015) Forest management type influences diversity and community composition of soil fungi across temperate forest ecosystems. Front Microbiol 6:1300. https://doi.org/10.3389/fmicb.2015.01300
Article PubMed PubMed Central Google Scholar
Grant S, Grant WD, Cowan DA, Jones BE, Ma Y, Ventosa A, Heaphy S (2006) Identification of eukaryotic open reading frames in metagenomic cDNA libraries made from environmental samples. Appl Environ Microbiol 72:135–143. https://doi.org/10.1128/AEM.72.1.135-143.2006
CAS Article PubMed PubMed Central Google Scholar
Gruninger RJ, Nguyen TTM, Reid ID, Yanke J, Wang P, Abbott DW, Tsang A, McAllister T (2018) Application of transcriptomics to compare the carbohydrate active enzymes that are expressed by diverse genera of anaerobic fungi to degrade plant cell wall carbohydrates. Front Microbiol 9:1581. https://doi.org/10.3389/fmicb.2018.01581
Article PubMed PubMed Central Google Scholar
Gubler U, Hoffman BJ (1983) A simple and very efficient method for generating cDNA libraries. Gene 25:263–269. https://doi.org/10.1016/0378-1119(83)90230-5
CAS Article PubMed Google Scholar
Gudynaite-Savitch L, White TC (2016) Fungal biotechnology for industrial enzyme production: focus on (Hemi) cellulase production strategies, advances and challenges. In: Schmoll M, Dattenböck C (eds) Gene expression systems in fungi: advancements and applications. Springer, Cham, pp 395–439. https://doi.org/10.1007/978-3-319-27951-0_19
Google Scholar
Guerriero G, Hausman JF, Strauss J, Ertan H, Siddiqui KS (2016) Lignocellulosic biomass: biosynthesis, degradation, and industrial utilization. Eng Life Sci 16:1–16
CAS Article Google Scholar
Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5:R245–R249. https://doi.org/10.1016/S1074-5521(98)90108-9
CAS Article PubMed Google Scholar
Hesse CN, Mueller RC, Vuyisich M, Gallegos-Graves LV, Gleasner CD, Zak DR, Kuske CR (2015) Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests. Front Microbiol 6:337. https://doi.org/10.3389/fmicb.2015.00337
Article PubMed PubMed Central Google Scholar
Hirsch PR, Mauchline TH, Clark IM (2010) Culture-independent molecular techniques for soil microbial ecology. Soil Biol Biochem 42:878–887. https://doi.org/10.1016/j.soilbio.2010.02.019
CAS Article Google Scholar
Hua ZS, Han YJ, Chen LX, Liu J, Hu M, Li SJ, Kuang JL, Chain PS, Huang LN, Shu WS (2015) Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. ISME J 9:1280. https://doi.org/10.1038/ismej.2014.212
CAS Article PubMed Google Scholar
Iost I, Dreyfus M (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J 14:3252
CAS Article Google Scholar
Jarque S, Bittner M, Blaha L, Hilscherova K (2016) Yeast biosensors for detection of environmental pollutants: current state and limitations. Trends Biotechnol 34:408–419. https://doi.org/10.1016/j.tibtech.2016.01.007
CAS Article PubMed Google Scholar
Jumpponen A, Johnson LC (2005) Can rDNA analyses of diverse fungal communities in soil and roots detect effects of environmental manipulations—a case study from tallgrass prairie. Mycologia 97:1177–1194. https://doi.org/10.1080/15572536.2006.11832728
CAS Article PubMed Google Scholar
Kellner H, Luis P, Portetelle D, Vandenbol M (2011) Screening of a soil metatranscriptomic library by functional complementation of Saccharomyces cerevisiae mutants. Microbiol Res 166:360–368. https://doi.org/10.1016/j.micres.2010.07.006
CAS Article PubMed Google Scholar
Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Bio 18:355–364. https://doi.org/10.1016/j.jtemb.2005.02.006
CAS Article Google Scholar
Kim J, Kim MS, Koh AY, Xie Y, Zhan X (2016) FMAP: functional mapping and analysis pipeline for metagenomics and metatranscriptomics studies. BMC Bioinform 17:420. https://doi.org/10.1186/s12859-016-1278-0
CAS Article Google Scholar
Knietsch A, Bowien S, Whited G, Gottschalk G, Daniel R (2003) Identification and characterization of coenzyme B12-dependent glycerol dehydratase-and diol dehydratase-encoding genes from metagenomic DNA libraries derived from enrichment cultures. Appl Environ Microbiol 69:3048–3060. https://doi.org/10.1128/AEM.69.6.3048-3060.2003
CAS Article PubMed PubMed Central Google Scholar
Koringa PG, Thakkar JR, Pandit RJ, Hinsu AT, Parekh MJ, Shah RK, Jakhesara SJ, Joshi CG (2019) Metagenomic characterisation of ruminal bacterial diversity in buffaloes from birth to adulthood using 16S rRNA gene amplicon sequencing. Funct Integr Genomics 19:237–247. https://doi.org/10.1007/s10142-018-0640-x
CAS Article PubMed Google Scholar
Kozdrój J, van Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405–1417. https://doi.org/10.1016/S0038-0717(00)00058-4
Article Google Scholar
Lara E, Berney C, Harms H, Chatzinotas A (2007) Cultivation-independent analysis reveals a shift in ciliate 18S rRNA gene diversity in a polycyclic aromatic hydrocarbon-polluted soil. FEMS Microbiol Ecol 62:365–373. https://doi.org/10.1111/j.1574-6941.2007.00387.x
CAS Article PubMed Google Scholar
Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15. https://doi.org/10.1016/j.ejsobi.2006.10.002
Article Google Scholar
Lehembre F, Doillon D, David E, Perrotto S, Baude J, Foulon J, Harfouche L, Vallon L, Poulain J, Da Silva C, Wincker P (2013) Soil metatranscriptomics for mining eukaryotic heavy metal resistance genes. Environ Microbiol 15:2829–2840. https://doi.org/10.1111/1462-2920.12143
CAS Article PubMed Google Scholar
Lehmann M, Riedel K, Adler K, Kunze G (2000) Amperometric measurement of copper ions with a deputy substrate using a novel Saccharomyces cerevisiae sensor. Biosens Bioelectron 15:211–219. https://doi.org/10.1016/S0956-5663(00)00060-9
CAS Article PubMed Google Scholar
Leimena MM, Ramiro-Garcia J, Davids M, van den Bogert B, Smidt H, Smid EJ, Boekhorst J, Zoetendal EG, Schaap PJ, Kleerebezem M (2013) A comprehensive metatranscriptome analysis pipeline and its validation using human small intestine microbiota datasets. BMC Genom 14:530. https://doi.org/10.1186/1471-2164-14-530
CAS Article Google Scholar
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809. https://doi.org/10.1038/nature04983
CAS Article PubMed Google Scholar
Liles MR, Manske BF, Bintrim SB, Handelsman J, Goodman RM (2003) A census of rRNA genes and linked genomic sequences within a soil metagenomic library. Appl Environ Microbiol 69:2684–2691. https://doi.org/10.1128/AEM.69.5.2684-2691.2003
CAS Article PubMed PubMed Central Google Scholar
Liu W, Stahl D (2007) Molecular approaches for the measurement of density, diversity, and phylogeny. In: Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (eds) Manual of environmental microbiology, 3rd edn. ASM Press, Washington DC, pp 139–156. https://dx.doi.org/10.1128/9781555815882.ch12
Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522
CAS Article Google Scholar
Luis P, Kellner H, Martin F, Buscot F (2005) A molecular method to evaluate basidiomycete laccase gene expression in forest soils. Geoderma 128:18–27. https://doi.org/10.1016/j.geoderma.2004.12.023
CAS Article Google Scholar
Ma A, Sun M, McDermaid A, Liu B, Ma Q (2019) MetaQUBIC: a computational pipeline for gene-level functional profiling of metagenome and metatranscriptome. Bioinformatics 35:4474–4477. https://doi.org/10.1093/bioinformatics/btz414
Article PubMed Google Scholar
Mantere T, Kersten S, Hoischen A (2019) Long-read sequencing emerging in medical genetics. Front Genet 10:426. https://doi.org/10.3389/fgene.2019.00426
CAS Article PubMed PubMed Central Google Scholar
Marmeisse R, Kellner H, Fraissinet-Tachet L, Luis P (2017) Discovering protein-coding genes from the environment: time for the eukaryotes? Trends Biotechnol 35:824–835. https://doi.org/10.1016/j.tibtech.2017.02.003
CAS Article PubMed Google Scholar
Marsh TL (1999) Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous populations of amplification products. Curr Opin Microbiol 2:323–327. https://doi.org/10.1016/S1369-5274(99)80056-3
CAS Article PubMed Google Scholar
Martinez X, Pozuelo M, Pascal V, Campos D, Gut I, Gut M, Azpiroz F, Guarner F, Manichanh C (2016) MetaTrans: an open-source pipeline for metatranscriptomics. Sci Rep 6:26447. https://doi.org/10.1038/srep26447
CAS Article PubMed PubMed Central Google Scholar
Matsuura H, Yamamoto Y, Muraoka M, Akaishi K, Hori Y, Uemura K, Tsuji N, Harada K, Hirata K, Bamba T, Miyasaka H (2013) Development of surface-engineered yeast cells displaying phytochelatin synthase and their application to cadmium biosensors by the combined use of pyrene-excimer fluorescence. Biotechnol Prog 29:1197–1202. https://doi.org/10.1002/btpr.1789
CAS Article PubMed Google Scholar
Medini D, Serruto D, Parkhill J, Relman DA, Donati C, Moxon R, Falkow S, Rappuoli R (2008) Microbiology in the post-genomic era. Nat Rev Microbiol 6:419–430. https://doi.org/10.1038/nrmicro1901
CAS Article PubMed Google Scholar
Mehra RK, Winge DR (1991) Metal ion resistance in fungi: molecular mechanisms and their regulated expression. J Cell Biochem 45:30–40. https://doi.org/10.1002/jcb.240450109
CAS Article PubMed PubMed Central Google Scholar
Miller DN, Bryant JE, Madsen EL, Ghiorse WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65:4715–4724
CAS Article Google Scholar
Minet M, Dufour ME, Lacroute F (1992) Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J 2:417–422. https://doi.org/10.1046/j.1365-313X.1992.t01-38-00999.x
CAS Article PubMed Google Scholar
Mitchell E, Frisbie S, Sarkar B (2011) Exposure to multiple metals from groundwater—a global crisis: geology, climate change, health effects, testing, and mitigation. Metallomics 3:874–908. https://doi.org/10.1039/C1MT00052G
CAS Article PubMed Google Scholar
Moran MA (2009) Metatranscriptomics: eavesdropping on complex microbial communities-large-scale sequencing of mRNAs retrieved from natural communities provides insights into microbial activities and how they are regulated. Microbe 4:329. https://doi.org/10.1128/microbe.4.329.1
Article Google Scholar
Mukherjee A, Yadav R, Marmeisse R, Fraissinet-Tachet L, Reddy MS (2019a) Heavy metal hypertolerant eukaryotic aldehyde dehydrogenase isolated from metal contaminated soil by metatranscriptomics approach. Biochimie 160:183–192. https://doi.org/10.1016/j.biochi.2019.03.010
CAS Article PubMed Google Scholar
Mukherjee A, Yadav R, Marmeisse R, Fraissinet-Tachet L, Reddy MS (2019b) Detoxification of toxic heavy metals by serine protease inhibitor isolated from polluted soil. Int Biodeterior Biodegrad 143:104718. https://doi.org/10.1016/j.ibiod.2019.104718
CAS Article Google Scholar
Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141. https://doi.org/10.1023/A:1000669317571
CAS Article PubMed Google Scholar
Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. https://doi.org/10.1046/j.1351-0754.2003.0556.x
Article Google Scholar
Narayanasamy S, Jarosz Y, Muller EE, Heintz-Buschart A, Herold M, Kaysen A, Laczny CC, Pinel N, May P, Wilmes P (2016) IMP: a pipeline for reproducible reference-independent integrated metagenomic and metatranscriptomic analyses. Genome Biol 17:260. https://doi.org/10.1186/s13059-016-1116-8
Article PubMed PubMed Central Google Scholar
Ni Y, Li J, Panagiotou G (2016) COMAN: a web server for comprehensive metatranscriptomics analysis. BMC Genom 17:622. https://doi.org/10.1186/s12864-016-2964-z
Article Google Scholar
Niehaus F, Gabor E, Wieland S, Siegert P, Maurer KH, Eck J (2011) Enzymes for the laundry industries: tapping the vast metagenomic pool of alkaline proteases. Microb Biotechnol 4:767–776. https://doi.org/10.1111/j.1751-7915.2011.00279.x
Article PubMed PubMed Central Google Scholar
Nüsslein K, Tiedje JM (1998) Characterization of the dominant and rare members of a young Hawaiian soil bacterial community with small-subunit ribosomal DNA amplified from DNA fractionated on the basis of its guanine and cytosine composition. Appl Environ Microbiol 64:1283–1289
Article Google Scholar
O'Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550. https://doi.org/10.1128/AEM.71.9.5544-5550.2005
CAS Article PubMed PubMed Central Google Scholar
Opel KL, Chung D, McCord BR (2010) A study of PCR inhibition mechanisms using real time PCR. J Forensic Sci 55:25–33. https://doi.org/10.1111/j.1556-4029.2009.01245.x
CAS Article PubMed Google Scholar
Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740. https://doi.org/10.1126/science.276.5313.734
CAS Article PubMed Google Scholar
Patel DD, Patel AK, Parmar NR, Shah TM, Patel JB, Pandya PR, Joshi CG (2014) Microbial and carbohydrate active enzyme profile of buffalo rumen metagenome and their alteration in response to variation in the diet. Gene 545:88–94. https://doi.org/10.1016/j.gene.2014.05.003
CAS Article PubMed Google Scholar
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562. https://doi.org/10.1038/nrmicro2831
CAS Article PubMed Google Scholar
Poretsky RS, Bano N, Buchan A, LeCleir G, Kleikemper J, Pickering M, Pate WM, Moran MA, Hollibaugh JT (2005) Analysis of microbial gene transcripts in environmental samples. Appl Environ Microbiol 71:4121–4126. https://doi.org/10.1128/AEM.71.7.4121-4126.2005
CAS Article PubMed PubMed Central Google Scholar
Radhika V, Milkevitch M, Audigé V, Proikas-Cezanne T, Dhanasekaran N (2005) Engineered Saccharomyces cerevisiae strain BioS-1, for the detection of water-borne toxic metal contaminants. Biotechnol Bioeng 90:29–35. https://doi.org/10.1002/bit.20344
CAS Article PubMed Google Scholar
Ranjard L, Nazaret S, Gourbière F, Thioulouse J, Linet P, Richaume A (2000) A soil microscale study to reveal the heterogeneity of Hg (II) impact on indigenous bacteria by quantification of adapted phenotypes and analysis of community DNA fingerprints. FEMS Microbiol Ecol 31:107–115. https://doi.org/10.1111/j.1574-6941.2000.tb00676.x
CAS Article PubMed Google Scholar
Redon E, Loubière P, Cocaign-Bousquet M (2005) Role of mRNA stability during genome-wide adaptation of Lactococcus lactis to carbon starvation. J Biol Chem 280:36380–36385. https://doi.org/10.1074/jbc.M506006200
CAS Article PubMed Google Scholar
Roane TM, Pepper IL (1999) Microbial responses to environmentally toxic cadmium. Microb Ecol 38:358–364. https://doi.org/10.1007/s002489901001
CAS Article PubMed Google Scholar
Roda A, Roda B, Cevenini L, Michelini E, Mezzanotte L, Reschiglian P, Hakkila K, Virta M (2011) Analytical strategies for improving the robustness and reproducibility of bioluminescent microbial bioreporters. Anal Bioanal Chem 401:201–211. https://doi.org/10.1007/s00216-011-5091-3
CAS Article PubMed Google Scholar
Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, MacNeil IA, Minor C, Tiong CL (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 66:2541–2547. https://doi.org/10.1128/AEM.66.6.2541-2547.2000
CAS Article PubMed PubMed Central Google Scholar
Rossman AY (1998) Protocols for an all taxa biodiversity inventory of fungi in a Costa Rican conservation area. Parkway Publishers, Inc., USA. https://doi.org/10.2307/3761287
Article Google Scholar
Sandaa RA, Torsvik V, Enger Ø, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251. https://doi.org/10.1111/j.1574-6941.1999.tb00652.x
CAS Article PubMed Google Scholar
Scherens B, Goffeau A (2004) The uses of genome-wide yeast mutant collections. Genome Biol 5:229. https://doi.org/10.1186/gb-2004-5-7-229
Article PubMed PubMed Central Google Scholar
Schloss PD, Handelsman J (2003) Biotechnological prospects from metagenomics. Curr Opin Biotechnol 14:303–310. https://doi.org/10.1016/S0958-1669(03)00067-3
CAS Article PubMed Google Scholar
Sequeira JC, Rocha M, Alves MM, Salvador AF (2019) MOSCA: an automated pipeline for integrated metagenomics and metatranscriptomics data analysis. Practical Applications of Computational Biology and Bioinformatics, 12th International Conference (Springer International Publishing). https://doi.org/10.1007/978-3-319-98702-6_2
Google Scholar
Seshadri R, Leahy SC, Attwood GT, Teh KH, Lambie SC, Cookson AL, Eloe-Fadrosh EA, Pavlopoulos GA, Hadjithomas M, Varghese NJ, Paez-Espino D (2018) Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nat Biotechnol 36:359. https://doi.org/10.1038/nbt.4110
CAS Article PubMed PubMed Central Google Scholar
Shakya M, Lo CC, Chain PS (2019) Advances and challenges in metatranscriptomic analysis. Front Genet 10:904. https://doi.org/10.3389/fgene.2019.00904
Article PubMed PubMed Central Google Scholar
Sharma R, Sharma PK (2018) Metatranscriptome sequencing and analysis of agriculture soil provided significant insights about the microbial community structure and function. Ecol Genet Genomics 6:9–15. https://doi.org/10.1016/j.egg.2017.10.001
CAS Article Google Scholar
Shetty RS, Deo SK, Liu Y, Daunert S (2004) Fluorescence-based sensing system for copper using genetically engineered living yeast cells. Biotechnol Bioeng 88:664–670. https://doi.org/10.1002/bit.20331
CAS Article PubMed Google Scholar
Singh DP, Prabha R, Gupta VK, Verma MK (2018) Metatranscriptome analysis deciphers multifunctional genes and enzymes linked with the degradation of aromatic compounds and pesticides in the wheat rhizosphere. Front Microbiol 9:1331. https://doi.org/10.3389/fmicb.2018.01331
Article PubMed PubMed Central Google Scholar
Sjostrom SL, Bai Y, Huang M, Liu Z, Nielsen J, Joensson HN, Svahn HA (2014) High-throughput screening for industrial enzyme production hosts by droplet microfluidics. Lab Chip 14:806–813. https://doi.org/10.1039/c3lc51202a
CAS Article PubMed Google Scholar
Smit E, Leeflang P, Wernars K (1997) Detection of shifts in microbial community structure and diversity in soil caused by copper contamination using amplified ribosomal DNA restriction analysis. FEMS Microbiol Ecol 23:249–261. https://doi.org/10.1111/j.1574-6941.1997.tb00407.x
CAS Article Google Scholar
Söllinger A, Tveit AT, Poulsen M, Noel SJ, Bengtsso M, Bernhardt J, Hellwing ALF, Lund P, Riedel K, Schleper C, Højberg O (2018) Holistic assessment of rumen microbiome dynamics through quantitative metatranscriptomics reveals multifunctional redundancy during key steps of anaerobic feed degradation. MSystems 3:e00038–e118. https://doi.org/10.1128/mSystems.00038-18
Article PubMed PubMed Central Google Scholar
Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80:735–746. https://doi.org/10.1111/j.1574-6941.2012.01343.x
CAS Article PubMed Google Scholar
Takasaki K, Miura T, Kanno M, Tamaki H, Hanada S, Kamagata Y, Kimura N (2013) Discovery of glycoside hydrolase enzymes in an avicel-adapted forest soil fungal community by a metatranscriptomic approach. PLoS ONE 8:e55485. https://doi.org/10.1371/journal.pone.0055485
CAS Article PubMed PubMed Central Google Scholar
Tamames J, Puente-Sanchez F (2019) SqueezeM, a highly portable, fully automatic metagenomic analysis pipeline. Front Microbiol 9:3349. https://doi.org/10.3389/fmicb.2018.03349
Article PubMed PubMed Central Google Scholar
Terry SA, Badhan A, Wang Y, Chaves AV, McAllister TA (2019) Fibre digestion by rumen microbiota—a review of recent metagenomic and metatranscriptomic studies. Can J Anim Sci 99:678–692. https://doi.org/10.1139/cjas-2019-0024
Article Google Scholar
Thakur B, Yadav R, Fraissinet-Tachet L, Marmeisse R, Reddy MS (2018) Isolation of multi-metal tolerant ubiquitin fusion protein from metal polluted soil by metatranscriptomic approach. J Microbiol Methods 152:119–125. https://doi.org/10.1016/j.mimet.2018.08.001
CAS Article PubMed Google Scholar
Thakur B, Yadav R, Vallon L, Marmeisse R, Fraissinet-Tachet L, Reddy MS (2019) Multi-metal tolerance of von Willebrand factor type D domain isolated from metal contaminated site by metatranscriptomics approach. Sci Total Environ 661:432–440. https://doi.org/10.1016/j.scitotenv.2019.01.201
CAS Article PubMed Google Scholar
Torsvik V, Sørheim R, Goksøyr J (1996) Total bacterial diversity in soil and sediment communities—a review. J Ind Microbiol Biotechnol 17:170–178. https://doi.org/10.1007/BF01574690
CAS Article Google Scholar
Tringe SG, Rubin EM (2005) Metagenomics: DNA sequencing of environmental samples. Nat Rev Genet 6:805–814. https://doi.org/10.1038/nrg1709
CAS Article PubMed Google Scholar
Urich T, Lanzén A, Qi J, Huson DH, Schleper C, Schuster SC (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3:e2527. https://doi.org/10.1371/journal.pone.0002527
CAS Article PubMed PubMed Central Google Scholar
Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74. https://doi.org/10.1126/science.1093857
Article PubMed Google Scholar
Vopálenská I, Váchová L, Palková Z (2015) New biosensor for detection of copper ions in water based on immobilized genetically modified yeast cells. Biosens Bioelectron 72:160–167. https://doi.org/10.1016/j.bios.2015.05.006
CAS Article PubMed Google Scholar
Warnecke F, Hess M (2009) A perspective: metatranscriptomics as a tool for the discovery of novel biocatalysts. J Biotech 142:91–95. https://doi.org/10.1016/j.jbiotec.2009.03.022
CAS Article Google Scholar
Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565. https://doi.org/10.1038/nature06269
CAS Article PubMed Google Scholar
Wasserman GA, Liu X, Factor-Litvak P, Gardner JM, Graziano JH (2008) Developmental impacts of heavy metals and undernutrition. Basic Clin Pharmacol Toxicol 102:212–217. https://doi.org/10.1111/j.1742-7843.2007.00187.x
CAS Article PubMed Google Scholar
Weidner S, Arnold W, Puhler A (1996) Diversity of uncultured microorganisms associated with the seagrass Halophila stipulacea estimated by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 62:766–771
CAS Article Google Scholar
Westreich ST, Kor I, Mills DA, Lemay DG (2016) SAMSA: a comprehensive metatranscriptome analysis pipeline. BMC Bioinform 17:399. https://doi.org/10.1186/s12859-016-1270-8
Article Google Scholar
Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S, Basham D (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880. https://doi.org/10.1038/nature724
CAS Article PubMed Google Scholar
Yadav RK, Barbi F, Ziller A, Luis P, Marmeisse R, Reddy MS, Fraissinet-Tachet L (2014) Construction of sized eukaryotic cDNA libraries using low input of total environmental metatranscriptomic RNA. BMC Biotechnol 14:80. https://doi.org/10.1186/1472-6750-14-80
CAS Article PubMed PubMed Central Google Scholar
Zhang Y, Zhang X, Zhang H, He Q, Zhou Q, Su Z, Zhang C (2009) Responses of soil bacteria to long-term and short-term cadmium stress as revealed by microbial community analysis. Bull Environ Contam Toxicol 82:367–372. https://doi.org/10.1007/s00128-008-9613-4
CAS Article PubMed Google Scholar
Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD (2001) Reverse transcriptase template switching: A SMART™ approach for full-length cDNA library construction. Biotechniques 30:892–897. https://doi.org/10.2144/01304pf02
CAS Article PubMed Google Scholar
Ziller A, Yadav RK, Capdevila M, Reddy MS, Vallon L, Marmeisse R, Atrian S, Palacios Ò, Fraissinet-Tachet L (2017) Metagenomics analysis reveals a new metallothionein family: sequence and metal-binding features of new environmental cysteine-rich proteins. J Inorg Biochem 167:1–11. https://doi.org/10.1016/j.jinorgbio.2016.11.017
CAS Article PubMed Google Scholar

Download references

Acknowledgements

Authors are thankful to Council of Scientific and Industrial Research, Govt. of India for sponsoring a research project on “Novel gene pool from copper polluted soil ecosystem using metatranscriptomic approach” under file No. 38(1425)/16/EMR-II.

Author information

Affiliations

Department of Biotechnology, Thapar Institute of Engineering and Technology, Patiala, Punjab, 147004, India
Arkadeep Mukherjee & M. Sudhakara Reddy

Authors

Arkadeep Mukherjee
View author publications
You can also search for this author in PubMed Google Scholar
M. Sudhakara Reddy
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Sudhakara Reddy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mukherjee, A., Reddy, M.S. Metatranscriptomics: an approach for retrieving novel eukaryotic genes from polluted and related environments. 3 Biotech 10, 71 (2020). https://doi.org/10.1007/s13205-020-2057-1

Download citation

Received: 29 March 2019
Accepted: 06 January 2020
Published: 27 January 2020
DOI: https://doi.org/10.1007/s13205-020-2057-1

Keywords

Metatranscriptomics
Eukaryotic genes
Toxic metal tolerance
Functional diversity
Microbiomes
Metagenomes