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Bacteria and Archaea Communities in Cerrado Natural Pond Sediments

  • Microbiology of Aquatic Systems
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Abstract

Natural ponds in the Brazilian Cerrado harbor high biodiversity but are still poorly studied, especially their microbial assemblage. The characterization of the microbial community in aquatic environments is fundamental for understanding its functioning, particularly under the increasing pressure posed by land conversion and climate change. Here, we aim to characterize the structure (abundance, richness, and diversity) and composition of the Bacteria and Archaea in the sediment of two natural ponds belonging to different basins that primarily differ in size and depth in the Cerrado. Sediment samples were collected in the dry and rainy seasons and the transition periods between both. The structure and composition of Bacteria and Archaea were assessed by 16S rRNA gene pyrosequencing. We identified 45 bacterial and four archaeal groups. Proteobacteria and Acidobacteria dominated the bacterial community, while Euryarchaeota and Thaumarchaeota dominated the archaeal community. Seasonal fluctuations in the relative abundance of microbial taxa were observed, but pond characteristics were more determinant to community composition differences. Microbial communities are highly diverse, and local variability could partially explain the microbial structure’s main differences. Functional predictions based in 16S rRNA gene accessed with Tax4Fun indicated an enriched abundance of predicted methane metabolism in the deeper pond, where higher abundance of methanogenic archaea Methanocella, Methanosaeta, and Methanomicrobiaceae was detected. Our dataset encompasses the more comprehensive survey of prokaryotic microbes in Cerrado’s aquatic environments. Here, we present basic and essential information about composition and diversity, for initial insights into the ecology of Bacteria and Archaea in these environments.

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Data Availability

The raw sequence data files were processed by NCBI SRA database and are accessible under the accession number PRJNA603538.

References

  1. Ribeiro JF, Walter BMT (2008) As principais fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: Ecologia e Flora1st edn. Embrapa Cerrados, Brasília, pp 152–212

    Google Scholar 

  2. Myers N, Myers N, Mittermeier RA et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501

    Article  CAS  PubMed  Google Scholar 

  3. Lima JEFW, Silva EM (2008) Recursos hídricos do bioma Cerrado: importância e situação. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: Ecologia e Flora1st edn. Embrapa Cerrados, Brasília, pp 90–106

    Google Scholar 

  4. Padovesi-Fonseca C (2005) Caracterização dos ecossistemas aquáticos do Cerrado. In: Scariot A, Souza-Silva JC, Felfili JM (eds) Cerrado: ecologia, biodiversidade e conservação1st edn. Ministério do Meio Ambiente, Brasília, pp 415–429

    Google Scholar 

  5. Sousa FDR, Elmoor-Loureiro LMA, De Mendonça-Galvão L (2013) Cladocerans (Crustacea, Anomopoda and Ctenopoda) from Cerrado of Central Brazil: inventory of phytophilous community in natural wetlands. Biota Neotrop 13:222–229. https://doi.org/10.1590/S1676-06032013000300025

    Article  Google Scholar 

  6. Gomes PP, Ibañez MDSR, de Freitas JS (2010) Spatial and temporal variation of Peridinium umbonatum F. Stein, 1883 (Dinophyceae) and its relationship with total phytoplankton of a shallow, oligotrophic lake in Central Brazil (Lagoon Bonita, Distrito Federal). Acta Limnol Bras 22:317–324. https://doi.org/10.1590/S2179-975X2010000300008

    Article  Google Scholar 

  7. Fonseca BM, Estrela LMB (2015) Desmídias perifíticas de cinco lagoas do Distrito Federal, Brasil: II - Gêneros Euastrum Ehrenberg ex Ralfs, Micrasterias C. Agardh ex Ralfs e Triploceras Bailey. Hoehnea 42:399–417. https://doi.org/10.1590/2236-8906-58/2014

    Article  Google Scholar 

  8. Fonseca BM, de Mendonça-Galvão L, Sousa FDR, Elmoor-Loureiro LMA, Gomes-e-Souza MB, Pinto RL, Petracco P, de Oliveira RC, de Jesus Lima E (2018) Biodiversity in pristine wetlands of Central Brazil: a multi-taxonomic approach. Wetlands 38:145–156. https://doi.org/10.1007/s13157-017-0964-7

    Article  Google Scholar 

  9. Prosser JI, Martiny JBH (2020) Conceptual challenges in microbial community ecology. Philos Trans R Soc B Biol Sci 375:20190241. https://doi.org/10.1098/rstb.2019.0241

    Article  Google Scholar 

  10. Widder S, Allen RJ, Pfeiffer T et al (2016) Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J 10:2557–2568. https://doi.org/10.1038/ismej.2016.45

    Article  PubMed  PubMed Central  Google Scholar 

  11. Zhang J, Yang Y, Zhao L, Li Y, Xie S, Liu Y (2015) Distribution of sediment bacterial and archaeal communities in plateau freshwater lakes. Appl Microbiol Biotechnol 99:3291–3302. https://doi.org/10.1007/s00253-014-6262-x

    Article  CAS  PubMed  Google Scholar 

  12. Liu Y, Zhang J, Zhao L, Li Y, Dai Y, Xie S (2015) Distribution of sediment ammonia-oxidizing microorganisms in plateau freshwater lakes. Appl Microbiol Biotechnol 99:4435–4444. https://doi.org/10.1007/s00253-014-6341-z

    Article  CAS  PubMed  Google Scholar 

  13. Wurzbacher C, Fuchs A, Attermeyer K, Frindte K, Grossart HP, Hupfer M, Casper P, Monaghan MT (2017) Shifts among eukaryota, bacteria, and archaea define the vertical organization of a lake sediment. Microbiome 5:41. https://doi.org/10.1186/S40168-017-0255-9

    Article  PubMed  PubMed Central  Google Scholar 

  14. Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U, Brodie EL, Williams KH, Hubbard SS, Banfield JF (2016) Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Comun 7:1–11. https://doi.org/10.1038/ncomms13219

    Article  CAS  Google Scholar 

  15. Pajares S, Bohannan BJM, Souza V (2016) Editorial: The role of microbial communities in tropical ecosystems. Front Microbiol 7:1805. https://doi.org/10.3389/fmicb.2016.01805

    Article  PubMed  PubMed Central  Google Scholar 

  16. Billard E, Domaizon I, Tissot N, Arnaud F, Lyautey E (2015) Multi-scale phylogenetic heterogeneity of archaea, bacteria, methanogens and methanotrophs in lake sediments. Hydrobiologia 751:159–173. https://doi.org/10.1007/s10750-015-2184-6

    Article  Google Scholar 

  17. Herber J, Klotz F, Frommeyer B, Weis S, Straile D, Kolar A, Sikorski J, Egert M, Dannenmann M, Pester M (2020) A single Thaumarchaeon drives nitrification in deep oligotrophic Lake Constance. Environ Microbiol 22:212–228. https://doi.org/10.1111/1462-2920.14840

    Article  CAS  PubMed  Google Scholar 

  18. Arce MI, von Schiller D, Bengtsson MM, Hinze C, Jung H, Alves RJE, Urich T, Singer G (2018) Drying and rainfall shape the structure and functioning of nitrifying microbial communities in riverbed sediments. Front Microbiol 9:2794. https://doi.org/10.3389/fmicb.2018.02794

    Article  PubMed  PubMed Central  Google Scholar 

  19. Bustamante M, Nardoto G, Pinto A, Resende JCF, Takahashi FSC, Vieira LCG (2012) Potential impacts of climate change on biogeochemical functioning of Cerrado ecosystems. Brazilian J Biol 72:655–671. https://doi.org/10.1590/S1519-69842012000400005

    Article  CAS  Google Scholar 

  20. Marengo JA, Jones R, Alves LM, Valverde MC (2009) Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system. Int J Climatol 29:2241–2255. https://doi.org/10.1002/joc.1863

    Article  Google Scholar 

  21. Feng B-W, Li X-R, Wang J-H, Hu ZY, Meng H, Xiang LY, Quan ZX (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol Ecol 70:236–248. https://doi.org/10.1111/j.1574-6941.2009.00772.x

    Article  CAS  Google Scholar 

  22. Naether A, Foesel BU, Naegele V, Wüst PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G, Gockel S, Hemp A, Kalko EKV, Linsenmair KE, Pfeiffer S, Renner S, Schöning I, Weisser WW, Wells K, Fischer M, Overmann J, Friedrich MW (2012) Environmental factors affect Acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406. https://doi.org/10.1128/AEM.01325-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Alvim EACC (2017) Variações sazonais e espaciais das concentrações elementares em compartimentos biogeoquímicos de lagoas naturais rasas do Cerrado e suas influências no funcionamento ecossistêmico. Tese, Universidade de Brasília

  24. Silva FAM, Assad ED, Evangelista BA (2008) Caracterização climática do bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: ecologia e flora1st edn. Embrapa Cerrados, Brasília, pp 70–88

    Google Scholar 

  25. Sousa FDR (2012) Diversidade da fauna de Cladocera (Crustacea, Branchiopoda) associada à macrófitas em áreas úmidas naturais do Cerrado do Brasil Central. Dissertação, Universidade de Brasília

  26. Bouyoucos GJ (1962) Hydrometer method improved for making particle size analysis of soils. Agron J 54:464–465

    Article  Google Scholar 

  27. Embrapa CN de P de S (1997) Manual de métodos de análise de solo, 2nd. Embrapa-CNPS. Documentos,1, Rio de Janeiro

  28. Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contracts soil microbial diversity. ISME J 1(4):283–290. https://doi.org/10.1038/ismej.2007.53

    Article  CAS  PubMed  Google Scholar 

  29. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7(9):668–669. https://doi.org/10.1038/nmeth0910-668b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  32. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, The Human Microbiome Consortium, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. https://doi.org/10.1101/gr.112730.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Price MN, Dehal PS, Arkin AP (2009) Computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650. https://doi.org/10.1093/molbev/msp077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hammer Ø (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9 http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed 11 Nov 2019

  35. Andersen KS, Kirkegaard RH, Karst SM, Albertsen M (2018) ampvis2: an R package to analyse and visualise 16S rRNA amplicon data. bioRxiv. https://doi.org/10.1101/299537

  36. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884. https://doi.org/10.1093/bioinformatics/btv287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Chong J, Liu P, Zhou G, Xia J (2020) Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc 15:799–821. https://doi.org/10.1038/s41596-019-0264-1

    Article  CAS  PubMed  Google Scholar 

  39. Rodrigues T, Catão E, Bustamante MMC, Quirino BF, Kruger RH, Kyaw CM (2014) Seasonal effects in a lake sediment archaeal community of the Brazilian savanna. Archaea 2014:1–9. https://doi.org/10.1155/2014/957145

    Article  CAS  Google Scholar 

  40. Dai Y, Yang Y, Wu Z, Feng Q, Xie S, Liu Y (2016) Spatiotemporal variation of planktonic and sediment bacterial assemblages in two plateau freshwater lakes at different trophic status. Appl Microbiol Biotechnol 100:4161–4175. https://doi.org/10.1007/s00253-015-7253-2

    Article  CAS  PubMed  Google Scholar 

  41. Dai Y, Wu J, Zhong F, Cui N, Kong L, Liang W, Cheng S (2019) Macrophyte identity shapes water column and sediment bacterial community. Hydrobiologia 835:71–82. https://doi.org/10.1007/s10750-019-3930-y

    Article  Google Scholar 

  42. Galand PE, Lucas S, Fagervold SK, Peru E, Pruski AM, Vétion G, Dupuy C, Guizien K (2016) Disturbance increases microbial community diversity and production in marine sediments. Front Microbiol 7:1950. https://doi.org/10.3389/fmicb.2016.01950

    Article  PubMed  PubMed Central  Google Scholar 

  43. Crowther TW, Thomas SM, Maynard DS, Baldrian P, Covey K, Frey SD, van Diepen LTA, Bradford MA (2015) Biotic interactions mediate soil microbial feedbacks to climate change. Proc Natl Acad Sci 112:7033–7038. https://doi.org/10.1073/pnas.1502956112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Comte J, Berga M, Severin I, Logue JB, Lindström ES (2017) Contribution of different bacterial dispersal sources to lakes: population and community effects in different seasons. Environ Microbiol 19:2391–2404. https://doi.org/10.1111/1462-2920.13749

    Article  CAS  PubMed  Google Scholar 

  45. Esteves FA (2011) Sedimentos límnicos. Fundamentos de limnologia3rd edn. Interciência, Rio de Janeiro, pp 339–354

    Google Scholar 

  46. Berdjeb L, Pollet T, Chardon C, Jacquet S (2013) Spatio-temporal changes in the structure of archaeal communities in two deep freshwater lakes. FEMS Microbiol Ecol 86:215–230. https://doi.org/10.1111/1574-6941.12154

    Article  CAS  PubMed  Google Scholar 

  47. Briée C, Moreira D, López-García P (2007) Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microbiol 158:213–227. https://doi.org/10.1016/j.resmic.2006.12.012

    Article  CAS  PubMed  Google Scholar 

  48. Marinho CC, Palma-silva C, Albertoni EF, Esteves FDA (2015) Emergent macrophytes alter the sediment composition in a small, shallow subtropical lake: implications for methane emission. Am J Plant Sci 6:315–322. https://doi.org/10.4236/ajps.2015.62036

    Article  CAS  Google Scholar 

  49. Dos Santos Fonseca AL, Cardoso Marinho C, De Assis Esteves F (2015) Aquatic macrophytes detritus quality and sulfate availability shape the methane production pattern in a dystrophic coastal lagoon. Am J Plant Sci 06:1675–1684. https://doi.org/10.4236/ajps.2015.610167

    Article  CAS  Google Scholar 

  50. Pereira de Castro A, Sartori da Silva MRS, Quirino BF, da Cunha Bustamante MM, Krüger RH (2016) Microbial diversity in Cerrado biome (Neotropical Savanna) Soils. PLoS One 11:e0148785. https://doi.org/10.1371/journal.pone.0148785

    Article  CAS  PubMed Central  Google Scholar 

  51. Catão E, Castro AP, Barreto CC, Krüger RH, Kyaw CM (2013) Diversity of Archaea in Brazilian savanna soils. Arch Microbiol 195:507–512. https://doi.org/10.1007/s00203-013-0882-x

    Article  CAS  PubMed  Google Scholar 

  52. Lindström K, Aserse AA, Mousavi SA (2015) Evolution and taxonomy of nitrogen-fixing organisms with emphasis on Rhizobia. In: Bruijn FJ (ed) Biological Nitrogen Fixation, vol 1. Wiley Blackwell, New Jersey, pp 21–86. https://doi.org/10.1002/9781119053095.ch3

    Chapter  Google Scholar 

  53. Isobe K, Ohte N (2014) Ecological perspectives on microbes involved in N-cycling. Microbes Environ 29:4–16. https://doi.org/10.1264/jsme2.ME13159

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00744

  55. Silva MRSS, Pereira de Castro A, Krüger RH, Bustamante M (2019) Soil bacterial communities in the Brazilian Cerrado: response to vegetation type and management. Acta Oecologica 100:103463. https://doi.org/10.1016/j.actao.2019.103463

    Article  Google Scholar 

  56. Liu FH, Lin GH, Gao G, Qin BQ, Zhang JS, Zhao GP, Zhou ZH, Shen JH (2009) Bacterial and archaeal assemblages in sediments of a large shallow freshwater lake, Lake Taihu, as revealed by denaturing gradient gel electrophoresis. J Appl Microbiol 106:1022–1032. https://doi.org/10.1111/j.1365-2672.2008.04069.x

    Article  CAS  PubMed  Google Scholar 

  57. Vissers EW, Blaga CI, Bodelier PLE, Muyzer G, Schleper C, Sinninghe Damsté JS, Tourna M, Laanbroek HJ (2013) Seasonal and vertical distribution of putative ammonia-oxidizing thaumarchaeotal communities in an oligotrophic lake. FEMS Microbiol Ecol 83:515–526. https://doi.org/10.1111/1574-6941.12013

    Article  CAS  PubMed  Google Scholar 

  58. Fan X, Xing P (2016) Differences in the composition of archaeal communities in sediments from contrasting zones of Lake Taihu. Front Microbiol 7:1510. https://doi.org/10.3389/fmicb.2016.01510

    Article  PubMed  PubMed Central  Google Scholar 

  59. de Araujo ASF, Bezerra WM, dos Santos VM, Rocha SMB, Carvalho NS, de Lyra MCCP, Figueiredo MVB, de Almeida Lopes ÂC, Melo VMM (2017) Distinct bacterial communities across a gradient of vegetation from a preserved Brazilian Cerrado. Antonie Van Leeuwenhoek 110:457–469. https://doi.org/10.1007/s10482-016-0815-1

    Article  PubMed  Google Scholar 

  60. Belmok A, Rodrigues-oliveira T, Lopes FAC et al (2019) Long-Term effects of periodical fires on archaeal communities from Brazilian Cerrado soils. Archaea 2019:1–11. https://doi.org/10.1155/2019/6957210

    Article  CAS  Google Scholar 

  61. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR (2018) Bacterial quorum sensing and microbial community Interactions. MBio 9. https://doi.org/10.1128/mBio.02331-17

  62. Berberich ME, Beaulieu JJ, Hamilton TL, Waldo S, Buffam I (2020) Spatial variability of sediment methane production and methanogen communities within a eutrophic reservoir: importance of organic matter source and quantity. Limnol Oceanogr 65:1336–1358. https://doi.org/10.1002/lno.11392

    Article  CAS  Google Scholar 

  63. Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, Tyson GW (2019) An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol 17:219–232. https://doi.org/10.1038/s41579-018-0136-7

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Michelle Wong for her suggestions for this work.

Funding

This work received financial support from the Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF, process number 193.000.567/2009), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq.

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Silveira, R., Silva, M.R.S.S., de Roure Bandeira de Mello, T. et al. Bacteria and Archaea Communities in Cerrado Natural Pond Sediments. Microb Ecol 81, 563–578 (2021). https://doi.org/10.1007/s00248-020-01574-x

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