Skip to main content

Advertisement

Log in

Viral metagenomics analysis and eight novel viral genomes identified from the Dushanzi mud volcanic soil in Xinjiang, China

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Viruses are the most abundant biological entities and play significant biological roles in marine system. However, little is known about their biodiversity in mud volcanic soil, which is salty and covered with emitting sludge. In this study, we report metagenomic analysis results of viral community composition and function from the Dushanzi mud volcanic soil (named NHS) in Xinjiang, China, and provide a comparative analysis with other environmental types.

Materials and methods

We utilized metagenomes to obtain the virus data and carried out viral automatic phylogenetic and functional analyses by the metagenomics analysis server. After assembling by metaSPAdes, scaffolds were rapidly identified and annotated with the PHAge Search Tool in order to identify new phage genomes.

Results and discussion

For the ssDNA viral group, Microviridae were the most abundant viral family, which were above 95%. Other plant viruses (Geminiviridae, Nanoviridae) and animal viruses (Circoviridae, Parvoviridae) were also detected. The majority of viral significant hits belonged to Siphoviridae (80.36%). Phages, which infect bacteria, were widely distributed in the soil sample. There were eight novel viral genomes identified in the NHS virome. The two longest scaffolds were annotated to Pseudomonas aeruginosa phage YMC11 and Acinetobacter baumannii phage LZ35, respectively. Other six new viral genomes were identified as Microviridae. Comparisons of NHS virome with other published viromes revealed that the type of ecosystem mainly drove the viral community structure.

Conclusions

This work provided detailed viral community composition and function information, which supplemented microbial community research on mud volcanoes. Importantly, we also identified eight complete viral genomes in the NHS virome which were obviously different from known viruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andam CP, Harlow TJ, Papke RT, Gogarten JP (2012) Ancient origin of the divergent forms of leucyl-tRNA synthetases in the Halobacteriales. BMC Evol Biol 12:1–14

    Article  CAS  Google Scholar 

  • Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Olson R, Parsons R, Rayhawk S, Suttle CA, Rohwer F (2006) The marine viromes of four oceanic regions. PLoS Biol 4:2121–2131

    Article  CAS  Google Scholar 

  • Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang YJ, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16–W21

    Article  CAS  Google Scholar 

  • Barber AJ, Tjokrosapoetro S, Charlton TR (1986) Mud volcanos, shale diapirs, wrench faults, and melanges in accretionary complexes, Eastern Indonesia. AAPG Bull 70:1729–1741

    Google Scholar 

  • Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2017) GenBank. Nucleic Acids Res 45:D37–D42

    Article  CAS  Google Scholar 

  • Brentlinger KL, Hafenstein S, Novak CR, Fane BA, Borgon R, McKenna R, Agbandje-McKenna M (2002) Microviridae, a family divided: isolation, characterization, and genome sequence of phi MH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J Bacteriol 184:1089–1094

    Article  CAS  Google Scholar 

  • Cai L, Zhang R, He Y, Feng X, Jiao N (2016) Metagenomic analysis of virioplankton of the subtropical Jiulong River estuary, China. Viruses 8:35

    Article  CAS  Google Scholar 

  • Carcer DAD, Lopez-Bueno A, Pearce DA, Alcami A (2015) Biodiversity and distribution of polar freshwater DNA viruses. Sci Adv 1:e1400127

    Article  CAS  Google Scholar 

  • Chen SC, Hsu SK, Wang Y, Chung SH, Chen PC, Tsai CH, Liu CS, Lin HS, Lee YW (2014) Distribution and characters of the mud diapirs and mud volcanoes off Southwest Taiwan. J Asian Earth Sci 92:201–214

    Article  Google Scholar 

  • Cita MB, Ryan WBF, Paggi L (1981) Prometheus mud breccia; an example of shale diapirism in the western Mediterrranean ridge. Ann Géol Pays Hellén 305:543–569

    Google Scholar 

  • Coelho FJRC, Louvado A, Domingues PM, Cleary DFR, Ferreira M, Almeida A, Cunha MR, Cunha A, Gomes NCM (2016) Integrated analysis of bacterial and microeukaryotic communities from differentially active mud volcanoes in the Gulf of Cadiz. Sci Rep-Uk 6:35272

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al (2010) QIIME allows analysis of highthroughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Corinaldesi C, Dell'Anno A, Danovaro R (2012) Viral infections stimulate the metabolism and shape prokaryotic assemblages in submarine mud volcanoes. ISME J 6:1250–1259

    Article  CAS  Google Scholar 

  • Cuylaerts M, Naudts L, Casier R, Khabuev AV, Belousov OV, Kononov EE, Khlystov O, De Batist M (2012) Distribution and morphology of mud volcanoes and other fluid flow-related Lake-bed structures in lake Baikal, Russia. Geo-Mar Lett 32:383–394

    Article  Google Scholar 

  • Dennehy JJ (2014) What ecologists can tell virologists. Annu Rev Microbiol 68:117–135

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    Article  CAS  Google Scholar 

  • Engelhardt T, Kallmeyer J, Cypionka H, Engelen B (2014) High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments. ISME J 8:1503–1509

    Article  Google Scholar 

  • Evans RJ, Stewart SA, Davies RJ (2008) The structure and formation of mud volcano summit calderas. J Geol Soc Lond 165:769–780

    Article  Google Scholar 

  • Garner SA, Everson JS, Lambden PR, Fane BA, Clarke IN (2004) Isolation, molecular characterisation and genome sequence of a bacteriophage (Chp3) from Chlamydophila pecorum. Virus Genes 28:207–214

    Article  CAS  Google Scholar 

  • Guo ZH, Huang HL, Wu XL, Hao YC, Su YB (2016) Complete genome sequence of lytic bacteriophage LZ35 infecting acinetobacter baumannii isolates. Genome Announc 4:e01104–e01116

    Article  Google Scholar 

  • Han LL, Yu DT, Zhang LM, Shen JP, He JZ (2017) Genetic and functional diversity of ubiquitous DNA viruses in selected Chinese agricultural soils. Sci Rep 7:45142

    Article  CAS  Google Scholar 

  • Hopkins M, Kailasan S, Cohen A, Roux S, Tucker KP, Shevenell A, Agbandje-McKenna M, Breitbart M (2014) Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J 8:2093–2103

    Article  CAS  Google Scholar 

  • Jensen LJ, Julien P, Kuhn M, von Mering C, Muller J, Doerks T, Bork P (2007) eggNOG: automated construction and annotation of orthologous groups of genes. Nucleic Acids Res 36:D250–D254

    Article  CAS  Google Scholar 

  • Jeon J, Kim JW, Yong D, Lee K, Chong Y (2012) Complete genome sequence of the bacteriophage YMC01/01/P52 PAE BP, which causes lysis of Verona integron-encoded metallo-beta-lactamase-producing, carbapenem-resistant pseudomonas aeruginosa. J Virol 86:13876–13877

    Article  CAS  Google Scholar 

  • Kanehisa M (2002) The KEGG database. Novartis Found Symp 247:91–103

    Article  CAS  Google Scholar 

  • Kim KH, Chang HW, Nam YD, Roh SW, Kim MS, Sung Y, Jeon CO, Oh HM, Bae JW (2008) Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl Environ Microb 74:5975–5985

    Article  CAS  Google Scholar 

  • Kopf A, Robertson AHF, Clennell MB, Flecker R (1998) Mechanisms of mud extrusion on the Mediterranean ridge accretionary complex. Geo-Mar Lett 18:97–114

    Article  Google Scholar 

  • Krupovic M, Forterre P (2011) Microviridae goes temperate: microvirus-related proviruses reside in the genomes of Bacteroidetes. PLoS One 6:e19893

    Article  CAS  Google Scholar 

  • Labonte JM, Suttle CA (2013) Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front Microbiol 4:404

    Article  Google Scholar 

  • Liu BL, Everson JS, Fane B, Giannikopoulou P, Vretou E, Lambden PR, Clarke IN (2000) Molecular characterization of a bacteriophage (Chp2) from Chlamydia psittaci. J Virol 74:3464–3469

    Article  CAS  Google Scholar 

  • Maniloff J, Ackermann HW (1998) Taxonomy of bacterial viruses: establishment of tailed virus genera and the order Caudovirales. Arch Virol 143:2051–2063

    Article  CAS  Google Scholar 

  • Markowitz VM, Ivanova NN, Szeto E, Palaniappan K, Chu K, Dalevi D, Chen IMA, Grechkin Y, Dubchak I, Anderson I, Lykidis A, Mavromatis K, Hugenholtz P, Kyrpides NC (2008) IMG/M a data management and analysis system for metagenomes. Nucleic Acids Res 36:D534–D538

    Article  CAS  Google Scholar 

  • Mascle J, Mary F, Praeg D, Brosolo L, Camera L, Ceramicola S, Dupre S (2014) Distribution and geological control of mud volcanoes and other fluid/free gas seepage features in the Mediterranean Sea and nearby Gulf of Cadiz. Geo-Mar Lett 34:89–110

    Article  CAS  Google Scholar 

  • Mazzini A, Svensen H, Planke S, Guliyev I, Akhmanov GG, Fallik T, Banks D (2009) When mud volcanoes sleep: insight from seep geochemistry at the Dashgil mud volcano, Azerbaijan. Mar Pet Geol 26:1704–1715

    Article  CAS  Google Scholar 

  • Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM et al (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:1–8

    Article  CAS  Google Scholar 

  • Milkov AV (2000) Worldwide distribution of submarine mud volcanoes and associated gas hydrates. Mar Geol 167:29–42

    Article  CAS  Google Scholar 

  • Milkov AV (2005) Global distribution of mud volcanoes and their significance in petroleum exploration as a source of methane in the atmosphere and hydrosphere and as a geohazard. Nato Sci S Ss Iv Ear 51:29–34

    Article  CAS  Google Scholar 

  • Moore JC, Vrolijk P (1992) Fluids in accretionary prisms. Rev Geophys 30:113–135

    Article  Google Scholar 

  • Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806–810

    Article  CAS  Google Scholar 

  • Nurk S, Meleshko D, Korobeynikov A, Pevzner PA (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27:824–834

    Article  CAS  Google Scholar 

  • Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a web browser. BMC Bioinformatics 12:1–10

    Article  Google Scholar 

  • Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY et al (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691–5702

    Article  CAS  Google Scholar 

  • Pachiadaki MG, Lykousis V, Stefanou EG, Kormas KA (2010) Prokaryotic community structure and diversity in the sediments of an active submarine mud volcano (Kazan mud volcano, East Mediterranean Sea). FEMS Microbiol Ecol 72:429–444

    Article  CAS  Google Scholar 

  • Pachiadaki MG, Kallionaki A, Dahlmann A, De Lange GJ, Kormas KA (2011) Diversity and spatial distribution of prokaryotic communities along a sediment vertical profile of a deep-sea mud volcano. Microb Ecol 62:655–668

    Article  Google Scholar 

  • Papke RT, Koenig JE, Rodriguez-Valera F, Doolittle WF (2004) Frequent recombination in a saltern population of Halorubrum. Science 306:1928–1929

    CAS  Google Scholar 

  • Papke RT, White E, Reddy P, Weigel G, Kamekura M, Minegishi H, Usami R, Ventosa A (2011) A multilocus sequence analysis approach to the phylogeny and taxonomy of the Halobacteriales. Int J Syst Evol Microbiol 61:2984–2995

    Article  CAS  Google Scholar 

  • Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq) a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:D61–D65

    Article  CAS  Google Scholar 

  • Quaiser A, Dufresne A, Ballaud F, Roux S, Zivanovic Y, Colombet J, Sime-Ngando T, Francez AJ (2015) Diversity and comparative genomics of Microviridae in Sphagnum-dominated peatlands. Front Microbiol 6:375

    Article  Google Scholar 

  • Reavy B, Swanson MM, Cock PJ, Dawson L, Freitag TE, Singh BK, Torrance L, Mushegian AR, Taliansky M (2015) Distinct circular single-stranded DNA viruses exist in different soil types. Appl Environ Microbiol 81:3934–3945

    Article  CAS  Google Scholar 

  • Ren J, Ahlgren NA, Lu YY, Fuhrman JA, Sun FZ (2017) VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 5:69

    Article  Google Scholar 

  • Renaudin J, Pascarel MC, Bove JM (1987) Spiroplasma virus-4-nucleotide-sequence of the viral-DNA, regulatory signals, and proposed genome organization. J Bacteriol 169:4950–4961

    Article  CAS  Google Scholar 

  • Rhodes ME, Spear JR, Oren A, House CH (2011) Differences in lateral gene transfer in hypersaline versus thermal environments. BMC Evol Biol 11:199

    Article  CAS  Google Scholar 

  • Roux S, Faubladier M, Mahul A, Paulhe N, Bernard A, Debroas D, Enault F (2011) Metavir: a web server dedicated to virome analysis. Bioinformatics 27:3074–3075

    Article  CAS  Google Scholar 

  • Roux S, Enault F, Robin A, Ravet V, Personnic S, Theil S, Colombet J, Sime-Ngando T, Debroas D (2012a) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7:e33641

    Article  CAS  Google Scholar 

  • Roux S, Krupovic M, Poulet A, Debroas D, Enault F (2012b) Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS One 7:e40418

    Article  CAS  Google Scholar 

  • Roux S, Enault F, Ravet V, Colombet J, Bettarel Y, Auguet JC, Bouvier T, Lucas-Staat S, Vellet A, Prangishvili D, Forterre P, Debroas D, Sime-Ngando T (2016) Analysis of metagenomic data reveals common features of halophilic viral communities across continents. Environ Microbiol 18:889–903

    Article  Google Scholar 

  • Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010

    Article  CAS  Google Scholar 

  • Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  CAS  Google Scholar 

  • Suttle CA (2007) Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  Google Scholar 

  • Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database an updated version includes eukaryotes. BMC Bioinformatics 4:41

    Article  Google Scholar 

  • Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6:1–11

    Article  Google Scholar 

  • Williamson KE, Wommack KE, Radosevich M (2003) Sampling natural viral communities from soil for culture-independent analyses. Appl Environ Microbiol 69:6628–6633

    Article  CAS  Google Scholar 

  • Williamson KE, Corzo KA, Drissi CL, Buckingham JM, Thompson CP, Helton RR (2013) Estimates of viral abundance in soils are strongly influenced by extraction and enumeration methods. Biol Fertil Soils 49:857–869

    Article  Google Scholar 

  • Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    Article  CAS  Google Scholar 

  • Yoshida M, Takaki Y, Eitoku M, Nunoura T, Takai K (2013) Metagenomic analysis of viral communities in (hado)pelagic sediments. PLoS One 8:e57271

    Article  CAS  Google Scholar 

  • Yu DT, Han LL, Zhang LM, He JZ (2017) Diversity and distribution characteristics of viruses in soils of a marine-terrestrial ecotone in East China. Microb Ecol 75:375–386

    Article  CAS  Google Scholar 

  • Zablocki O, van Zyl L, Adriaenssens EM, Rubagotti E, Tuffin M, Cary SC, Cowan D (2014) High-level dof tailed phages, eukaryote-associated viruses, and virophage-like elements in the metaviromes of Antarctic soils. Appl Environ Microbiol 80:6888–6897

    Article  CAS  Google Scholar 

  • Zablocki O, Adriaenssens EM, Cowan D (2016) Diversity and ecology of viruses in hyperarid desert soils. Appl Environ Microbiol 82:770–777

    Article  CAS  Google Scholar 

  • Zhao YL, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, Ellisman M, Deerinck T, Sullivan MB, Giovannoni SJ (2013) Abundant SAR11 viruses in the ocean. Nature 494:357–360

    Article  CAS  Google Scholar 

  • Zhou Y, Liang YJ, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:347–352

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Associate Professor Phillip Michael Chalk (The University of Melbourne) for improving English expression.

Funding

This work was supported by the National Science Foundation of China (Grant Nos. 41571248 and 41771289).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Li-Li Han.

Additional information

Responsible editor: Huaiying Yao

Electronic supplementary material

ESM 1

(PPTX 324 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, DT., He, JZ., Zhang, LM. et al. Viral metagenomics analysis and eight novel viral genomes identified from the Dushanzi mud volcanic soil in Xinjiang, China. J Soils Sediments 19, 81–90 (2019). https://doi.org/10.1007/s11368-018-2045-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-018-2045-9

Keywords

Navigation