Abstract
The response of freshwater bacterial community to anthropogenic disturbance has been well documented, yet the studies of freshwater archaeal community are rare, especially in lotic environments. Here, we investigated planktonic and benthic archaeal communities in a human-perturbed watershed (Jiulong River Watershed, JRW) of southeast China by using Illumina 16S ribosomal RNA gene amplicon sequencing. The results of taxonomic assignments indicated that SAGMGC-1, Methanobacteriaceae, Methanospirillaceae, and Methanoregulaceae were the four most abundant families in surface waters, accounting for 12.65, 23.21, 18.58 and 10.97 % of planktonic communities, whereas Nitrososphaeraceae and Miscellaneous Crenarchaeotic Group occupied more than 49 % of benthic communities. The compositions of archaeal communities and populations in waters and sediments were significantly different from each other. Remarkably, the detection frequencies of families Methanobacteriaceae and Methanospirillaceae, and genera Methanobrevibacter and Methanosphaera in planktonic communities correlated strongly with bacterial fecal indicator, suggesting some parts of methanogenic Archaea may come from fecal contamination. Because soluble reactive phosphorus (SRP) and the ratio of dissolved inorganic nitrogen to SRP instead of nitrogen nutrients showed significant correlation with several planktonic Nitrosopumilus- and Nitrosotalea-like OTUs, Thaumarchaeota may play an unexplored role in biogeochemical cycling of river phosphorus. Multivariate statistical analyses revealed that the variation of α-diversity of planktonic archaeal community was best explained by water temperature, whereas nutrient concentrations and stoichiometry were the significant drivers of β-diversity of planktonic and benthic communities. Taken together, these results demonstrate that the structure of archaeal communities in the JRW is sensitive to anthropogenic disturbances caused by riparian human activities.
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References
Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105(Supplement 1):11512–11519. doi:10.1073/pnas.0801925105
Auguet JC, Casamayor EO (2008) A hotspot for cold Crenarchaeota in the neuston of high mountain lakes. Environ Microbiol 10(4):1080–1086. doi:10.1111/j.1462-2920.2007.01498.x
Auguet JC, Casamayor EO (2013) Partitioning of Thaumarchaeota populations along environmental gradients in high mountain lakes. FEMS Microbiol Ecol 84(1):154–164. doi:10.1111/1574-6941.12047
Auguet JC, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4(2):182–190. doi:10.1038/ismej.2009.109
Auguet JC, Nomokonova N, Camarero L, Casamayor EO (2011) Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes. Appl Environ Microbiol 77(6):1937–45. doi:10.1128/AEM.01213-10
Bai Y, Qi W, Liang J, Qu J (2014) Using high-throughput sequencing to assess the impacts of treated and untreated wastewater discharge on prokaryotic communities in an urban river. Appl Microbiol Biotechnol 98(4):1841–51. doi:10.1007/s00253-013-5116-2
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(2):215–230. doi:10.1111/1574-6941.12154
Blanchet F, Legendre P (2010) AEM: tools to construct asymmetric eigenvector maps (AEM) spatial variables. R package version 03-2/r88
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89(9):2623–2632, http://dx.doi.org/10.1890/07-0986.1
Bogard MJ, del Giorgio PA, Boutet L, Chaves MCG, Prairie YT, Merante A, Derry AM (2014) Oxic water column methanogenesis as a major component of aquatic CH4 fluxes. Nat Commun 5:5350. doi:10.1038/ncomms6350
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6(3):245–252. doi:10.1038/nrmicro1852
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7(5):335–336. doi:10.1038/nmeth.f.303
Chaban B, Ng SYM, Jarrell KF (2006) Archaeal habitats—from the extreme to the ordinary. Can J Microbiol 52(2):73–116. doi:10.1139/w05-147
Chen N, Peng B, Hong H, Turyaheebwa N, Cui S, Mo X (2013) Nutrient enrichment and N: P ratio decline in a coastal bay-river system in southeast China: the need for a dual nutrient (N and P) management strategy. Ocean Coast Manage 81:7–13. doi:10.1016/j.ocecoaman.2012.07.013
Dang H, Zhou H, Yang J, Ge H, Jiao N, Luan X, Zhang C, Klotz MG (2013) Thaumarchaeotal signature gene distribution in sediments of the northern South China Sea: an indicator of the metabolic intersection of the marine carbon, nitrogen, and phosphorus cycles? Appl Environ Microbiol 79(7):2137–47. doi:10.1128/AEM.03204-12
Diniz JAF, Bini LM (2005) Modelling geographical patterns in species richness using eigenvector-based spatial filters. Glob Ecol Biogeogr 14(2):177–185. doi:10.1111/j.1466-822X.2005.00147.x
Durbin AM, Teske A (2012) Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Front Microbiol 3:168. doi:10.3389/fmicb.2012.00168
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. doi:10.1093/bioinformatics/btq461
Fisher JC, Newton RJ, Dila DK, McLellan SL (2015) Urban microbial ecology of a freshwater estuary of Lake Michigan. Elementa 3(1):000064. doi:10.12952/journal.elementa.000064
Galand PE, Lovejoy C, Vincent WF (2006) Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat Microb Ecol 44(2):115–126. doi:10.3354/ame044115
Galand PE, Casamayor EO, Kirchman DL, Potvin M, Lovejoy C (2009) Unique archaeal assemblages in the Arctic Ocean unveiled by massively parallel tag sequencing. ISME J 3:860–869. doi:10.1038/ismej.2009.23
Grossart HP, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. Proc Natl Acad Sci U S A 108(49):19657–19661. doi:10.1073/pnas.1110716108
Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 108(52):21206–11. doi:10.1073/pnas.1109000108
Hayden CJ, Beman JM (2015) Microbial diversity and community structure along a lake elevation gradient in Yosemite National Park, California. USA Environ Microbiol. doi:10.1111/1462-2920.12938
Herfort L, Kim JH, Coolen MJL, Abbas B, Schouten S, Herndl GJ, Damste JSS (2009) Diversity of Archaea and detection of crenarchaeotal amoA genes in the rivers Rhine and Têt. Aquat Microb Ecol 55(2):189–201. doi:10.3354/ame01294
Herrmann M, Saunders AM, Schramm A (2008) Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl Environ Microbiol 74(10):3279–3283. doi:10.1128/Aem.02802-07
Hollibaugh JT, Gifford SM, Moran MA, Ross MJ, Sharma S, Tolar BB (2014) Seasonal variation in the metratranscriptomes of a Thaumarchaeota population from SE USA coastal waters. ISME J 8(3):685–698. doi:10.1038/ismej.2013.171
Hu A, Yao T, Jiao N, Liu Y, Yang Z, Liu X (2010) Community structures of ammonia-oxidising archaea and bacteria in high-altitude lakes on the Tibetan Plateau. Freshw Biol 55(11):2375–2390. doi:10.1111/j.1365-2427.2010.02454.x
Hu A, Yang X, Chen N, Hou L, Ma Y, Yu CP (2014) Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci Total Environ 472:746–756. doi:10.1016/j.scitotenv.2013.11.097
Hu A, Hou L, Yu CP (2015) Biogeography of planktonic and benthic archaeal communities in a subtropical eutrophic estuary of China. Microb Ecol 70(2):322–335. doi:10.1007/s00248-015-0597-4
Huang J, Li Q, Pontius RG, Klemas V, Hong H (2011) Detecting the dynamic linkage between landscape characteristics and water quality in a subtropical coastal watershed, southeast China. Environ Manag 51(1):32–44. doi:10.1007/s00267-011-9793-2
Hugoni M, Agogue H, Taib N, Domaizon I, Mone A, Galand PE, Bronner G, Debroas D, Mary I (2015a) Temporal dynamics of active prokaryotic nitrifiers and archaeal communities from river to sea. Microb Ecol 70(2):473–83. doi:10.1007/s00248-015-0601-z
Hugoni M, Domaizon I, Taib N, Biderre-Petit C, Agogue H, Galand PE, Debroas D, Mary I (2015b) Temporal dynamics of active Archaea in oxygen-depleted zones of two deep lakes. Environ Microbiol Rep 7(2):321–9. doi:10.1111/1758-2229.12251
Jiang HC, Dong HL, Deng SC, Yu BS, Huang QY, Wu QL (2009) Response of Archaeal community structure to environmental changes in lakes on the Tibetan Plateau, Northwestern China. Geomicrobiol J 26(4):289–297. doi:10.1080/01490450902892662
Johnston C, Ufnar JA, Griffith JF, Gooch JA, Stewart JR (2010) A real-time qPCR assay for the detection of the nifH gene of Methanobrevibacter smithii, a potential indicator of sewage pollution. J Appl Microbiol 109(6):1946–1956. doi:10.1111/j.1365-2672.2010.04824.x
Keough BP, Schmidt TM, Hicks RE (2003) Archaeal nucleic acids in picoplankton from great lakes on three continents. Microb Ecol 46(2):238–248. doi:10.1007/s00248-003-1003-1
Kim S (2012) ppcor: partial and semi-partial (Part) correlation. http://pa/package=ppcor
Korajkic A, Parfrey LW, McMinn BR, Baeza YV, VanTeuren W, Knight R, Shanks OC (2015) Changes in bacterial and eukaryotic communities during sewage decomposition in Mississippi river water. Water Res 69:30–39. doi:10.1016/j.watres.2014.11.003
Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189. doi:10.1196/annals.1419.019
Liu LM, Yang J, Zhang YY (2011) Genetic diversity patterns of microbial communities in a subtropical riverine ecosystem (Jiulong River, southeast China). Hydrobiologia 678(1):113–125. doi:10.1007/s10750-011-0834-x
Liu J, Soininen J, Han BP, Declerck SAJ (2013a) Effects of connectivity, dispersal directionality and functional traits on the metacommunity structure of river benthic diatoms. J Biogeogr 40(12):2238–2248. doi:10.1111/jbi.12160
Liu S, Shen L, Lou L, Tian G, Zheng P, Hu B (2013b) Spatial distribution and factors shaping the niche segregation of ammonia-oxidizing microorganisms in the Qiantang River, China. Appl Environ Microbiol 79(13):4065–71. doi:10.1128/AEM.00543-13
Massana R, DeLong EF, Pedros-Alio C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microbiol 66(5):1777–1787. doi:10.1128/AEM.66.5.1777-1787.2000
Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson G, Solymos P, Stevens M, Wagner H (2009) vegan: community ecology package. R package version 115–2
Oton EV, Quince C, Nicol GW, Prosser JI, Gubry-Rangin C (2015) Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota. ISME J. doi:10.1038/ismej.2015.101
Parks DH, Mankowski T, Zangooei S, Porter MS, Armanini DG, Baird DJ, Langille MG, Beiko RG (2013) GenGIS 2: geospatial analysis of traditional and genetic biodiversity, with new gradient algorithms and an extensible plugin framework. PLoS One 8(7):e69885. doi:10.1371/journal.pone.0069885
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87(10):2614–25, http://dx.doi.org/10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2
Porat I, Vishnivetskaya TA, Mosher JJ, Brandt CC, Yang ZMK, Brooks SC, Liang LY, Drake MM, Podar M, Brown SD, Palumbo AV (2010) Characterization of Archaeal community in contaminated and uncontaminated surface stream sediments. Microb Ecol 60(4):784–795. doi:10.1007/s00248-010-9734-2
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(Database issue):D590–D596. doi:10.1093/nar/gks1219
Rangel TF, Diniz JAF, Bini LM (2010) SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 33(1):46–50. doi:10.1111/j.1600-0587.2009.06299.x
Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499(7459):431–437. doi:10.1038/nature12352
Saengkerdsub S, Ricke SC (2014) Ecology and characteristics of methanogenic archaea in animals and humans. Crit Rev Microbiol 40(2):97–116. doi:10.3109/1040841X.2013.763220
Santoro AE, Dupont CL, Richter RA, Craig MT, Carini P, McIlvin MR, Yang Y, Orsi WD, Moran DM, Saito MA (2015) Genomic and proteomic characterization of “Candidatus Nitrosopelagicus brevis”: an ammonia-oxidizing archaeon from the open ocean. Proc Natl Acad Sci U S A 112(4):1173–1178. doi:10.1073/pnas.1416223112
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. doi:10.1128/AEM.01541-09
Shade A, Peter H, Allison SD, Baho DL, Berga M, Burgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417. doi:10.3389/fmicb.2012.00417
Sokol ER, Herbold CW, Lee CK, Cary SC, Barrett JE (2013) Local and regional influences over soil microbial metacommunities in the Transantarctic Mountains. Ecosphere 4(11):art136. http://dx.doi.org/10.1890/ES13-00136.1
Souffreau C, Gucht KVD, Gremberghe I, Kosten S, Lacerot G, Lobão LM, Huszar VLM, Roland F, Jeppesen E, Vyverman W, Meester LD (2015) Environmental rather than spatial factors structure bacterioplankton communities in shallow lakes along a >6000 km latitudinal gradient in South America. Environ Microbiol 17(7):2336–2351. doi:10.1111/1462-2920.12692
Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl DA, Wagner M, Schleper C (2010) Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18(8):331–340. doi:10.1016/j.tim.2010.06.003
Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101. doi:10.1146/annurev-micro-092611-150128
Staley C, Gould TJ, Wang P, Phillips J, Cotner JB, Sadowsky MJ (2015) Species sorting and seasonal dynamics primarily shape bacterial communities in the Upper Mississippi River. Sci Total Environ 505:435–445. doi:10.1016/j.scitotenv.2014.10.012
Sun W, Xia C, Xu M, Guo J, Sun G, Wang A (2014) Community structure and distribution of planktonic ammonia-oxidizing archaea and bacteria in the Dongjiang River, China. Res Microbiol 165(8):657–70. doi:10.1016/j.resmic.2014.08.003
Tamames J, Abellan JJ, Pignatelli M, Camacho A, Moya A (2010) Environmental distribution of prokaryotic taxa. BMC Microbiol 10:85. doi:10.1186/1471-2180-10-85
Tang KW, McGinnis DF, Frindte K, Bruchert V, Grossart HP (2014) Paradox reconsidered: methane oversaturation in well-oxygenated lake waters. Limnol Oceanogr 59(1):275–284. doi:10.4319/lo.2014.59.1.0275
Teske A, Sørensen KB (2007) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2(1):3–18. doi:10.1038/ismej.2007.90
Ufnar JA, Wang SY, Ufnar DF, Ellender RD (2007) Methanobrevibacter ruminantium as an indicator of domesticated-ruminant fecal pollution in surface waters. Appl Environ Microbiol 73(21):7118–7121. doi:10.1128/AEM.00911-07
Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5(4):316–323. doi:10.1038/nrmicro1619
Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSG, Chan PP, Gollabgir A (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci U S A 107(19):8818–8823. doi:10.1073/pnas.0913533107
Wang S, Dong RM, Dong CZ, Huang L, Jiang H, Wei Y, Feng L, Liu D, Yang G, Zhang C, Dong H (2012) Diversity of microbial plankton across the Three Gorges Dam of the Yangtze River, China. Geosci Front 3(3):335–349. doi:10.1016/j.gsf.2011.11.013
Wang JJ, Shen J, Wu YC, Tu C, Soininen J, Stegen JC, He JZ, Liu XQ, Zhang L, Zhang EL (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7(7):1310–1321. doi:10.1038/ismej.2013.30
Wang Y, Liu L, Chen H, Yang J (2015) Spatiotemporal dynamics and determinants of planktonic bacterial and microeukaryotic communities in a Chinese subtropical river. Appl Microbiol Biotechnol. doi:10.1007/s00253-015-6773-0
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87(12):4576–4579. doi:10.1073/pnas.87.12.4576
Zhang J, Yang Y, Zhao L, Li Y, Xie S, Liu Y (2015a) Distribution of sediment bacterial and archaeal communities in plateau freshwater lakes. Appl Microbiol Biotechnol 99(7):3291–302. doi:10.1007/s00253-014-6262-x
Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL (2015b) Comprehensive evaluation of antibiotics emission and fate in the River Basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ Sci Technol 49(11):6772–6782. doi:10.1021/acs.est.5b00729
Zhou HW, Li DF, Tam NFY, Jiang XT, Zhang H, Sheng HF, Qin J, Liu X, Zou F (2011) BIPES, a cost-effective high-throughput method for assessing microbial diversity. ISME J 5(4):741–749. doi:10.1038/ismej.2010.160
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We thank Mr. Xiaoyong Yang for assistance in preparing samples for Illumina sequencing.
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This work was supported by the National Natural Science Foundation of China (31470539 and 41106096), Natural Science Foundation of Fujian Province, China (2013J05057), and the Knowledge Innovation Program of the Chinese Academy of Sciences (IUEQN201307).
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Hu, A., Wang, H., Li, J. et al. Archaeal community in a human-disturbed watershed in southeast China: diversity, distribution, and responses to environmental changes. Appl Microbiol Biotechnol 100, 4685–4698 (2016). https://doi.org/10.1007/s00253-016-7318-x
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DOI: https://doi.org/10.1007/s00253-016-7318-x