Time-resolved microbial guild responses to tidal cycling in a coastal acid-sulfate system
Yu-Chen Ling A , Han Ming Gan B , Michelle Bush C , Richard Bush D and John W. Moreau A E
+ Author Affiliations
- Author Affiliations
A School of Earth Sciences, University of Melbourne, Parkville, Vic. 3010, Australia.
B Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong 3220, Australia.
C Southern Cross GeoScience, Southern Cross University, Lismore, NSW 2480, Australia.
D International Centre for Balanced Land Use, The University of Newcastle, NSW 2308, Australia.
E Corresponding author. Email: jmoreau@unimelb.edu.au
Environmental Chemistry 15(2) 2-17 https://doi.org/10.1071/EN16203
Submitted: 9 December 2016 Accepted: 7 May 2017 Published: 22 March 2018
Environmental context. Microbes play key roles in controlling acidification and metal toxicity in coastal acid-sulfate soils. We characterised the time-dependent metabolic activities of abundant and rare taxa in acidifying tidal wetlands and showed that rare taxa exhibiting higher activity may exert significant influence on iron- and sulfur-cycling. Our findings yield new insights into the drivers and timing of iron- and sulfur-cycling in coastal acid-sulfate systems.
Abstract. Tidal inundation has been trialled as a remediation strategy for coastal acid-sulfate soil (CASS) environments. Microbial community structure and activity are hypothesised to play key roles in this process, but remain poorly understood for long-term (decadal or longer) CASS ecosystems. More detailed understanding of the distribution and timing of microbial activity in CASS ecosystems is necessary to evaluate their real bioremediation potential. In this study, we compared 16S ribosomal DNA (rRNA) and RNA (as copy DNA, cDNA, a proxy for overall enzymatic activity) sequence datasets to characterise and resolve microbial community structure and activity across a tidal cycle in the East Trinity long-term CASS wetland (Queensland, Australia). The timing and extent of activity among abundant (>1 %) and rare (<0.1 %) microbial taxa showed that a larger number of rare members (phylotype) displayed greater overall range in activity than was apparent for more abundant members. Certain taxa from both abundant and rare populations varied rapidly in their 16S rRNA levels in response to tidal cycling. The observation of rRNA accumulation in response to drying and rewetting was used to divide the microbial community structure into ‘early responders’ (within 3 h of dry-down or wet-up) and ‘delayed responders’ (3+ h after wet-up). Response patterns were phylogenetically constrained across supra- to subtidal zones across all tidal stages. Microbial iron- and sulfur-cycling networks included these rare but active taxa, illustrating their spatiotemporal complexity, which should be considered for an accurate assessment of bioremediation efficiency, and specially for validating predictive biogeochemical models of long-term CASS ecosystems.
Additional keywords: biogeochemistry.
References
[1] J. Shamshuddin, S. Muhrizal, I. Fauziah, M. Husni, Effects of adding organic materials to an acid sulfate soil on the growth of cocoa (Theobroma cacao L.) seedlings Sci. Total Environ. 2004, 323, 33.| Effects of adding organic materials to an acid sulfate soil on the growth of cocoa (Theobroma cacao L.) seedlingsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivFyiu7g%3D&md5=fafa53a0af4206dec7f7424f400665a3CAS |
[2] A. S. Kinsela, M. D. Melville, Mechanisms of acid sulfate soil oxidation and leaching under sugarcane cropping Soil Res. 2004, 42, 569.
| Mechanisms of acid sulfate soil oxidation and leaching under sugarcane croppingCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslSgsr0%3D&md5=4f9065dab034bc3b03be90f8c5f92fb6CAS |
[3] I. White, L. Heath, M. Melville, Ecological impacts of flood mitigation and drainage in coastal lowlands Aust. J. Emerg. Manag. 1999, 14, 9.
[4] R. W. Fitzpatrick, B. Powell, S. Marvanek, Atlas of Australian acid sulfate soils, in Inland Acid Sulfate Soil Systems across Australia (Eds R. Fitzpatrick, P. Shand) 2008, pp. 75–89 (CSIRO: Bentley, WA).
[5] L. Q. Minh, T. P. Tuong, M. Van Mensvoort, J. Bouma, Contamination of surface water as affected by land use in acid sulfate soils in the Mekong River Delta, Vietnam Agric. Ecosyst. Environ. 1997, 61, 19.
| Contamination of surface water as affected by land use in acid sulfate soils in the Mekong River Delta, VietnamCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtlOqs7g%3D&md5=d7bff6705da7ea9d5db0a02d6c15016aCAS |
[6] B. Powell, M. Martens, A review of acid sulfate soil impacts, actions and policies that impact on water quality in Great Barrier Reef catchments, including a case study on remediation at East Trinity Mar. Pollut. Bull. 2005, 51, 149.
| A review of acid sulfate soil impacts, actions and policies that impact on water quality in Great Barrier Reef catchments, including a case study on remediation at East TrinityCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitF2gtL0%3D&md5=648b672d32ad6b329b6a2f9ee6531e9aCAS |
[7] S. G. Johnston, A. F. Keene, E. D. Burton, R. T. Bush, L. A. Sullivan, Quantifying alkalinity generating processes in a tidally remediating acidic wetland Chem. Geol. 2012, 304–305, 106.
| Quantifying alkalinity generating processes in a tidally remediating acidic wetlandCrossref | GoogleScholarGoogle Scholar |
[8] B. Indraratna, A. Golab, W. Glamore, B. Blunden, Acid sulphate soil remediation techniques on the Shoalhaven River floodplain, Australia Q. J. Eng. Geol. Hydrogeol. 2005, 38, 129.
| Acid sulphate soil remediation techniques on the Shoalhaven River floodplain, AustraliaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFSisbc%3D&md5=43bdb71d2f66d3d52f5ef81f0692622dCAS |
[9] D. Dent, Acid Sulphate Soils: A Baseline for Research and Development 1986 (International Institute for Land Reclamation and Improvement: Wageningen).
[10] E. D. Burton, R. T. Bush, L. A. Sullivan, Acid-volatile sulfide oxidation in coastal flood plain drains: iron–sulfur cycling and effects on water quality Environ. Sci. Technol. 2006, 40, 1217.
| Acid-volatile sulfide oxidation in coastal flood plain drains: iron–sulfur cycling and effects on water qualityCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xlt1OgtQ%3D%3D&md5=ccf1ed34d8510b45d8048acc45af9907CAS |
[11] F. J. Stephens, M. Ingram, Two cases of fish mortality in low pH, aluminium rich water J. Fish Dis. 2006, 29, 765.
| Two cases of fish mortality in low pH, aluminium rich waterCrossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28jjt1Whtw%3D%3D&md5=63072d22c0cdb5a4320de1d6203542b7CAS |
[12] J. J. B. Bronswijk, J. E. Groenenberg, C. J. Ritsema, A. L. M. van Wijk, K. Nugroho, Evaluation of water management strategies for acid sulphate soils using a simulation model: a case study in Indonesia Agric. Water Manage. 1995, 27, 125.
| Evaluation of water management strategies for acid sulphate soils using a simulation model: a case study in IndonesiaCrossref | GoogleScholarGoogle Scholar |
[13] O. T. Denmead, B. C. T. Macdonald, G. Bryant, I. White, W. Wang, P. Moody, R. C. Dalal, W. Stainlay, Greenhouse gas emissions from sugarcane soils and nitrogen fertiliser management: II, in Proceedings of the 2006 Conference of the Australian Society of Sugar Cane Technologists, Mackay, Qld, 2–5 May 2006 (Ed. D. M. Hogarth).
[14] B. Macdonald, O. T. Denmead, I. White, Natural sulfur dioxide emissions from sulfuric soils Atmos. Environ. 2004, 38, 1473.
| Natural sulfur dioxide emissions from sulfuric soilsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVeiu7g%3D&md5=03afdc5240f8ea64b793e403416aed53CAS |
[15] S. G. Johnston, P. Slavich, P. Hirst, The acid flux dynamics of two artificial drains in acid sulfate soil backswamps on the Clarence River floodplain, Australia Aust. J. Soil Res. 2004, 42, 623.
| The acid flux dynamics of two artificial drains in acid sulfate soil backswamps on the Clarence River floodplain, AustraliaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslSgs74%3D&md5=e99dd2d5d2cb5f67560ac58133a56e77CAS |
[16] S. G. Johnston, E. D. Burton, R. T. Bush, A. F. Keene, L. A. Sullivan, D. Smith, A. E. McElnea, C. R. Ahern, B. Powell, Abundance and fractionation of Al, Fe and trace metals following tidal inundation of a tropical acid sulfate soil Appl. Geochem. 2010, 25, 323.
| Abundance and fractionation of Al, Fe and trace metals following tidal inundation of a tropical acid sulfate soilCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1Ohtbs%3D&md5=22401f4749017f0bcf2d27979d6b5d4aCAS |
[17] K. Ljung, F. Maley, A. Cook, P. Weinstein, Acid sulfate soils and human health – a millennium ecosystem assessment Environ. Int. 2009, 35, 1234.
| Acid sulfate soils and human health – a millennium ecosystem assessmentCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtF2lu7zE&md5=5d56546cee25be8f11fd242ffb8c6a97CAS |
[18] S. G. Johnston, A. F. Keene, E. D. Burton, R. T. Bush, L. A. Sullivan, A. E. McElnea, C. R. Ahern, C. D. Smith, B. Powell, R. K. Hocking, Arsenic mobilization in a seawater inundated acid sulfate soil Environ. Sci. Technol. 2010, 44, 1968.
| Arsenic mobilization in a seawater inundated acid sulfate soilCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFKitLk%3D&md5=e6d4fcae16b9cd2d01daa8669cc04285CAS |
[19] E. D. Burton, R. T. Bush, L. A. Sullivan, S. G. Johnston, R. K. Hocking, Mobility of arsenic and selected metals during re-flooding of iron- and organic-rich acid-sulfate soil Chem. Geol. 2008, 253, 64.
| Mobility of arsenic and selected metals during re-flooding of iron- and organic-rich acid-sulfate soilCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFejurs%3D&md5=6d62ff2d1c7ff2df008f1b950c5bf5b7CAS |
[20] W. Andriesse, M. E. F. Van Mensvoort, Acid sulfate soils: distribution and extent, in Encyclopedia of Soil Science (Ed. R. Lal) 2006, pp. 4–19 (Taylor & Francis: New York).
[21] J. W. Moreau, J. H. Fournelle, J. F. Banfield, Quantifying heavy metals sequestration by sulfate-reducing bacteria in an acid mine drainage-contaminated natural wetland Front. Microbiol. 2013, 4, 43.
| Quantifying heavy metals sequestration by sulfate-reducing bacteria in an acid mine drainage-contaminated natural wetlandCrossref | GoogleScholarGoogle Scholar |
[22] I. White, M. D. Melville, B. P. Wilson, J. Sammut, Reducing acidic discharges from coastal wetlands in eastern Australia Wetlands Ecol. Manage. 1997, 5, 55.
| Reducing acidic discharges from coastal wetlands in eastern AustraliaCrossref | GoogleScholarGoogle Scholar |
[23] Y.-C. Ling, J. W. Moreau, L. Berwick, S. Tulipani, K. Grice, R. Bush, Distribution of iron- and sulfate-reducing bacteria across a coastal acid sulfate soil (CASS) environment: implications for passive bioremediation by tidal inundation Front. Microbiol. 2015, 6, 624.
| Distribution of iron- and sulfate-reducing bacteria across a coastal acid sulfate soil (CASS) environment: implications for passive bioremediation by tidal inundationCrossref | GoogleScholarGoogle Scholar |
[24] R. Logares, S. Audic, D. Bass, L. Bittner, C. Boutte, R. Christen, J. M. Claverie, J. Decelle, J. R. Dolan, M. Dunthorn, B. Edvardsen, Patterns of rare and abundant marine microbial eukaryotes Curr. Biol. 2014, 24, 813.
| Patterns of rare and abundant marine microbial eukaryotesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXls1elsbY%3D&md5=e04699d2e190a843b8bc9e7dc9ea359bCAS |
[25] J. T. Lennon, S. E. Jones, Microbial seed banks: the ecological and evolutionary implications of dormancy Nat. Rev. Microbiol. 2011, 9, 119.
| Microbial seed banks: the ecological and evolutionary implications of dormancyCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFeguw%3D%3D&md5=0bf65a44333b4a3a101ef4430d10ec5eCAS |
[26] S. E. Jones, J. T. Lennon, Dormancy contributes to the maintenance of microbial diversity Proc. Natl. Acad. Sci. USA 2010, 107, 5881.
| Dormancy contributes to the maintenance of microbial diversityCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kktr8%3D&md5=74d7334c3763873b2b6e36d5fda903f7CAS |
[27] L. Wilhelm, K. Besemer, C. Fasching, T. Urich, G. A. Singer, C. Quince, T. J. Battin, Rare but active taxa contribute to community dynamics of benthic biofilms in glacier-fed streams Environ. Microbiol. 2014, 16, 2514.
| Rare but active taxa contribute to community dynamics of benthic biofilms in glacier-fed streamsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht12gtbrM&md5=6a82fc8a80ad69a47be4b3f58fec056eCAS |
[28] Z. T. Aanderud, S. E. Jones, N. Fierer, J. T. Lennon, Resuscitation of the rare biosphere contributes to pulses of ecosystem activity Front. Microbiol. 2015, 6, 1.
| Resuscitation of the rare biosphere contributes to pulses of ecosystem activityCrossref | GoogleScholarGoogle Scholar |
[29] A. Gobet, S. I. Böer, S. M. Huse, J. E. E. van Beusekom, C. Quince, M. L. Sogin, A. Boetius, A. Ramette, Diversity and dynamics of rare and of resident bacterial populations in coastal sands ISME J. 2012, 6, 542.
| Diversity and dynamics of rare and of resident bacterial populations in coastal sandsCrossref | GoogleScholarGoogle Scholar |
[30] J. Sjostedt, P. Koch-Schmidt, M. Pontarp, B. Canback, A. Tunlid, P. Lundberg, Å. Hagström, L. Riemann, Recruitment of members from the rare biosphere of marine bacterioplankton communities after an environmental disturbance Appl. Environ. Microbiol. 2012, 78, 1361.
| Recruitment of members from the rare biosphere of marine bacterioplankton communities after an environmental disturbanceCrossref | GoogleScholarGoogle Scholar |
[31] C. Pedrós-Alió, The rare bacterial biosphere Annu. Rev. Mar. Sci. 2012, 4, 449.
| The rare bacterial biosphereCrossref | GoogleScholarGoogle Scholar |
[32] M. S. Elshahed, N. H. Youssef, A. M. Spain, C. Sheik, F. Z. Najar, L. O. Sukharnikov, B. A. Roe, J. P. Davis, P. D. Schloss, V. L. Bailey, L. R. Krumholz, Novelty and uniqueness patterns of rare members of the soil biosphere Appl. Environ. Microbiol. 2008, 74, 5422.
| Novelty and uniqueness patterns of rare members of the soil biosphereCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2ru7vP&md5=e0edc6585b65a3ea75887dc0e07095f8CAS |
[33] J. A. Fuhrman, Microbial community structure and its functional implications Nature 2009, 459, 193.
| Microbial community structure and its functional implicationsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFShu70%3D&md5=c60fc261518be97cad008b808901e340CAS |
[34] D. L. Kirchman, M. T. Cottrell, C. Lovejoy, The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes Environ. Microbiol. 2010, 12, 1132.
| The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntFyitrY%3D&md5=828cd0356e791355854b875cf5309384CAS |
[35] C. Pedrós-Alió, Marine microbial diversity: can it be determined? Trends Microbiol. 2006, 14, 257.
| Marine microbial diversity: can it be determined?Crossref | GoogleScholarGoogle Scholar |
[36] S. A. Placella, E. L. Brodie, M. K. Firestone, Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Proc. Natl. Acad. Sci. USA 2012, 109, 10931.
| Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groupsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCit7bI&md5=1feaaaa9a27a968a79a163e5285ee8d6CAS |
[37] K. M. DeAngelis, W. L. Silver, A. W. Thompson, M. K. Firestone, Microbial communities acclimate to recurring changes in soil redox potential status Environ. Microbiol. 2010, 12, 3137.
| Microbial communities acclimate to recurring changes in soil redox potential statusCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlejtw%3D%3D&md5=41d20ad96c9c9845dbe9aa42d241be2bCAS |
[38] K. Ma, R. Conrad, Y. Lu, Responses of methanogen mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soil Appl. Environ. Microbiol. 2012, 78, 445.
| Responses of methanogen mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soilCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvFOrtw%3D%3D&md5=92b4ddef7751fda3605fbc085ac66870CAS |
[39] W. Borken, E. Matzner, Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils Glob. Change Biol. 2009, 15, 808.
| Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soilsCrossref | GoogleScholarGoogle Scholar |
[40] M. Van Gestel, R. Merckx, K. Vlassak, Microbial biomass responses to soil drying and rewetting: the fate of fast-and slow-growing microorganisms in soils from different climates Soil Biol. Biochem. 1993, 25, 109.
| Microbial biomass responses to soil drying and rewetting: the fate of fast-and slow-growing microorganisms in soils from different climatesCrossref | GoogleScholarGoogle Scholar |
[41] J. Zhou, B. Xia, D. S. Treves, L.-Y. Wu, T. L. Marsh, R. V. O’Neill, A. V. Palumbo, J. M. Tiedje, Spatial and resource factors influencing high microbial diversity in soil Appl. Environ. Microbiol. 2002, 68, 326.
| Spatial and resource factors influencing high microbial diversity in soilCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1WmtQ%3D%3D&md5=5aa9983c9314be4e72ee56b2a7f01977CAS |
[42] Y. C. Ling, Y. J. Chen, C. H. Sun, T. W. Cheng, P. L. Wang, L.-H. Lin, Potential of microbial methane formation in a high-temperature hydrocarbon seep Appl. Geochem. 2012, 27, 1666.
| Potential of microbial methane formation in a high-temperature hydrocarbon seepCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvFKrt78%3D&md5=bb62e64570773f40fb2cab477abca0aaCAS |
[43] C. Chenu, Y. Le Bissonnais, D. Arrouays, Organic matter influence on clay wettability and soil aggregate stability Soil Sci. Soc. Am. J. 2000, 64, 1479.
| Organic matter influence on clay wettability and soil aggregate stabilityCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsF2hsrs%3D&md5=4f09cf3b939529efb4bd5b9c2d89aa7bCAS |
[44] QASSIT, East Trinity Property Acid Sulfate Soils Remediation Action Plan: For Public Consultation 2000 (Queensland Government Department of Natural Resources: Brisbane).
[45] W. Hicks, G. Bowman, R.W. Fitzaptrick, East Trinity Acid Sulfate Soils: Part 1: Environmental Hazards 1999 (CSIRO Publishing: Adelaide).
[46] S. G. Johnston, A. F. Keene, R. T. Bush, E. D. Burton, L. A. Sullivan, L. Isaacson, A. E. McElnea, C. R. Ahern, C. D. Smith, B. Powell, Iron geochemical zonation in a tidally inundated acid sulfate soil wetland Chem. Geol. 2011, 280, 257.
| Iron geochemical zonation in a tidally inundated acid sulfate soil wetlandCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtVKisw%3D%3D&md5=7fdd3fe0b4f24f228178f8d3a32f60f6CAS |
[47] S. Johnston, A. Keene, R. Bush, Remediation of coastal acid sulfate soils by tidal inundation: effectiveness and geochemical implications, in Proceedings of 18th NSW Coastal Conference, Ballina, NSW, 3–6 November 2009, East Coast Conferences, Coffs Harbour, NSW.
[48] E. D. Burton, R. T. Bush, S. G. Johnston, L. A. Sullivan, Sulfur biogeochemical cycling and novel Fe–S mineralization pathways in a tidally re-flooded wetland Geochim. Cosmochim. Acta 2011, 75, 3434.
| Sulfur biogeochemical cycling and novel Fe–S mineralization pathways in a tidally re-flooded wetlandCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtVWnt78%3D&md5=9610da1ce79fb3bdb8617b7412ea10e5CAS |
[49] S. G. Johnston, A. F. Keene, R. T. Bush, L. A. Sullivan, V. N. L. Wong, Tidally driven water column hydro-geochemistry in a remediating acidic wetland J. Hydrol. 2011, 409, 128.
| Tidally driven water column hydro-geochemistry in a remediating acidic wetlandCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlaqu7jI&md5=4f3130ef73876232ca8f2b704c8155e7CAS |
[50] J. R. Pérez-Jiménez, L. Y. Young, L. J. Kerkhof, Molecular characterization of sulfate-reducing bacteria in anaerobic hydrocarbon-degrading consortia and pure cultures using the dissimilatory sulfite reductase (dsrAB) genes FEMS Microbiol. Ecol. 2001, 35, 145.
| Molecular characterization of sulfate-reducing bacteria in anaerobic hydrocarbon-degrading consortia and pure cultures using the dissimilatory sulfite reductase (dsrAB) genesCrossref | GoogleScholarGoogle Scholar |
[51] J. Geets, B. Borremans, L. Diels, D. Springael, J. Vangronsveld, D. van der Lelie, K. Vanbroekhoven, DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria J. Microbiol. Methods 2006, 66, 194.
| DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteriaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFGgt7o%3D&md5=5f319faf611176d7418285981ce83f40CAS |
[52] J. Reeder, R. Knight, The ‘rare biosphere’: a reality check Nat. Methods 2009, 6, 636.
| The ‘rare biosphere’: a reality checkCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKjsbbE&md5=2529ee74aa6167439b20608e99191075CAS |
[53] C. Quince, A. Lanzén, T. P. Curtis, R. J. Davenport, N. Hall, I. M. Head, L. F. Read, W. T. Sloan, Accurate determination of microbial diversity from 454 pyrosequencing data Nat. Methods 2009, 6, 639.
| Accurate determination of microbial diversity from 454 pyrosequencing dataCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1ahtL0%3D&md5=fe3f91c6a40684495b91c8ea0f82256eCAS |
[54] V. Kunin, A. Engelbrektson, H. Ochman, P. Hugenholtz, Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates Environ. Microbiol. 2010, 12, 118.
| Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimatesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFaisb4%3D&md5=588dc3521da8deed9cb3a33a37f5df4cCAS |
[55] P. D. Schloss, S. L. Westcott, Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis Appl. Environ. Microbiol. 2011, 77, 3219.
| Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysisCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXns1Sltrg%3D&md5=298e8a83caceceb57783b90138e26f84CAS |
[56] P. D. Schloss, D. Gevers, S. L. Westcott, Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies PLoS One 2011, 6, e27310.
| Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studiesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFejtA%3D%3D&md5=0ba8c3eb9f25d106567253fe76e31a7fCAS |
[57] P. D. Schloss, S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, B. B. Oakley, D. H. Parks, C. J. Robinson, J. W. Sahl, Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities Appl. Environ. Microbiol. 2009, 75, 7537.
| Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communitiesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1yltw%3D%3D&md5=81cbe7e0970b466f1b5f19eb1891f3f4CAS |
[58] J. J. Kozich, S. L. Westcott, N. T. Baxter, S. K. Highlander, P. D. Schloss, Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform Appl. Environ. Microbiol. 2013, 79, 5112.
| Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platformCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlSgu73L&md5=de47cd3a8f7d151076e296d81330e890CAS |
[59] R. C. Edgar, B. J. Haas, J. C. Clemente, C. Quince, R. Knight, UCHIME improves sensitivity and speed of chimera detection Bioinformatics 2011, 27, 2194.
| UCHIME improves sensitivity and speed of chimera detectionCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVSiurvL&md5=dd1e7e5103229f550716d90029405d6bCAS |
[60] J. R. Cole, Q. Wang, J. A. Fish, B. Chai, D. M. McGarrell, Y. Sun, C. T. Brown, A. Porras-Alfaro, C. R. Kuske, J. M. Tiedje, Ribosomal Database Project: data and tools for high throughput rRNA analysis Nucleic Acids Res. 2014, 42, D633.
| Ribosomal Database Project: data and tools for high throughput rRNA analysisCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslGk&md5=95ce7d5b18a25310a2724706f34b457eCAS |
[61] J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, QIIME allows analysis of high-throughput community sequencing data Nat. Methods 2010, 7, 335.
| QIIME allows analysis of high-throughput community sequencing dataCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFalurg%3D&md5=61a97b52f3ec5fc88ce6897a58acd128CAS |
[62] M. J. Claesson, O. O’Sullivan, Q. Wang, J. Nikkilä, J. R. Marchesi, H. Smidt, W. M. de Vos, R. P. Ross, P. W. O’Toole, Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine PLoS One 2009, 4, e6669.
| Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestineCrossref | GoogleScholarGoogle Scholar |
[63] Q. Wang, G. M. Garrity, J. M. Tiedje, J. R. Cole, Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy Appl. Environ. Microbiol. 2007, 73, 5261.
| Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomyCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsleqtrc%3D&md5=8fc4f900e0b24d0f9f5d25d762836bd4CAS |
[64] M. G. Dumont, C. Luke, Y. Deng, Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN Front. Microbiol. 2014, 5, 34.
| Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGANCrossref | GoogleScholarGoogle Scholar |
[65] A. L. Müller, K. U. Kjeldsen, T. Rattei, M. Pester, A. Loy, Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases ISME J. 2015, 9, 1152.
| Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductasesCrossref | GoogleScholarGoogle Scholar |
[66] E. D. Burton, L. A. Sullivan, R. T. Bush, S. G. Johnston, A. F. Keene, A simple and inexpensive chromium-reducible sulfur method for acid-sulfate soils Appl. Geochem. 2008, 23, 2759.
| A simple and inexpensive chromium-reducible sulfur method for acid-sulfate soilsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGnsLjK&md5=34556349afacef81018aed2c338ef466CAS |
[67] E. D. Burton, R. T. Bush, L. A. Sullivan, R. K. Hocking, D. R. Mitchell, S. G. Johnston, R. W. Fitzpatrick, M. Raven, S. McClure, L. Y. Jang, Iron-monosulfide oxidation in natural sediments: resolving microbially mediated S transformations using XANES, electron microscopy, and selective extractions Environ. Sci. Technol. 2009, 43, 3128.
| Iron-monosulfide oxidation in natural sediments: resolving microbially mediated S transformations using XANES, electron microscopy, and selective extractionsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFKktLo%3D&md5=59c2c5ea3ed3a5ade0ad08a98589fc85CAS |
[68] S. R. Claff, L. A. Sullivan, E. D. Burton, R. T. Bush, A sequential extraction procedure for acid sulfate soils: partitioning of iron Geoderma 2010, 155, 224.
| A sequential extraction procedure for acid sulfate soils: partitioning of ironCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlWgtbs%3D&md5=1dccfff88354474d886d8c85d7716bc3CAS |
[69] L. L. Stookey, Ferrozine – a new spectrophotometric reagent for iron Anal. Chem. 1970, 42, 779.
| Ferrozine – a new spectrophotometric reagent for ironCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXkt1WjtL8%3D&md5=f28651781ed0742e62dc0c86e02933efCAS |
[70] T. B. To, D. K. Nordstrom, K. M. Cunningham, J. W. Ball, R. B. McCleskey, New method for the direct determination of dissolved Fe (III) concentration in acid mine waters Environ. Sci. Technol. 1999, 33, 807.
| New method for the direct determination of dissolved Fe (III) concentration in acid mine watersCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXks1Kltg%3D%3D&md5=9c9842553979f890fcc62e658f2ec380CAS |
[71] E. Viollier, P. W. Inglett, K. Hunter, A. N. Roychoudhury, P. Van Cappellen, The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters Appl. Geochem. 2000, 15, 785.
| The ferrozine method revisited: Fe(II)/Fe(III) determination in natural watersCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsVWhsLc%3D&md5=fc08a5cb098508f297b6243272db694aCAS |
[72] L. Kerkhof, B. B. Ward, Comparison of nucleic acid hybridization and fluorometry for measurement of the relationship between RNA/DNA ratio and growth rate in a marine bacterium Appl. Environ. Microbiol. 1993, 59, 1303.
| 1:CAS:528:DyaK3sXksVGjsL4%3D&md5=8b9967e1de338660ec8828d9318f73e7CAS |
[73] S. J. Blazewicz, R. L. Barnard, R. A. Daly, M. K. Firestone, Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses ISME J. 2013, 7, 2061.
| Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and usesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1yit7nO&md5=106c609f59d83c6ba50a2a1b38c15928CAS |
[74] T. Hoehler, Biological energy requirements as quantitative boundary conditions for life in the subsurface Geobiology 2004, 2, 205.
| Biological energy requirements as quantitative boundary conditions for life in the subsurfaceCrossref | GoogleScholarGoogle Scholar |
[75] J. Evans, L. Sheneman, J. Foster, Relaxed neighbor joining: a fast distance-based phylogenetic tree construction method J. Mol. Evol. 2006, 62, 785.
| Relaxed neighbor joining: a fast distance-based phylogenetic tree construction methodCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xlt1Oisrs%3D&md5=16bfa1fd7ccbc32c5a927a712479872cCAS |
[76] L. Sheneman, J. Evans, J. A. Foster, Clearcut: a fast implementation of relaxed neighbor joining Bioinformatics 2006, 22, 2823.
| Clearcut: a fast implementation of relaxed neighbor joiningCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFyqt77K&md5=d38a1236234040960c8ee2c2c36c986cCAS |
[77] I. Letunic, P. Bork, Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Bioinformatics 2007, 23, 127.
| Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlGktLzN&md5=63d0e0aaa8d716a77aee416ae463ddbbCAS |
[78] I. Letunic, P. Bork, Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy Nucleic Acids Res. 2011, 39, W475.
| Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easyCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVOnu7w%3D&md5=524011210046a457bd713d804124a20aCAS |
[79] K. Faust, J. F. Sathirapongsasuti, J. Izard, N. Segata, D. Gevers, J. Raes, C. Huttenhower, Microbial co-occurrence relationships in the human microbiome PLOS Comput. Biol. 2012, 8, e1002606.
| Microbial co-occurrence relationships in the human microbiomeCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOnsLvK&md5=6777733c44c3afd357ebcca5bf2088e6CAS |
[80] P. Shannon, A. Markiel, O. Ozier, N. S. Baliga, J. T. Wang, D. Ramage, N. Amin, B. Schwikowski, T. Ideker, Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13, 2498.
| Cytoscape: a software environment for integrated models of biomolecular interaction networksCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFWrtr4%3D&md5=02c662221f68eee5349704acdec99d94CAS |
[81] G. Billon, Chemical speciation of sulfur compounds in surface sediments from three bays (Fresnaye, Seine and Authie) in northern France, and identification of some factors controlling their generation Talanta 2001, 53, 971.
| Chemical speciation of sulfur compounds in surface sediments from three bays (Fresnaye, Seine and Authie) in northern France, and identification of some factors controlling their generationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntFOgsw%3D%3D&md5=fd1eb18515976b40b458efb7214fc3c0CAS |
[82] A. Rambaut, FigTree v1. 4. Molecular Evolution, Phylogenetics and Epidemiology 2012 (University of Edinburgh, Institute of Evolutionary Biology: Edinburgh, UK).
[83] R Core Team, R: A Language and Environment for Statistical Computing 2009 (R Foundation for Statistical Computing: Vienna, Austria).
[84] G.R. Warnes, B. Bolker, L. Bonebakker, R. Gentleman, W. Huber, A. Liaw, T. Lumley, M. Maechler, A. Magnusson, S. Moeller, M. Schwartz, gplots: Various R Programming Tools for Plotting Data. R Package Version 2 2009.
[85] E. Paradis, J. Claude, K. Strimmer, APE: Analyses of phylogenetics and evolution in R language Bioinformatics 2004, 20, 289.
| APE: Analyses of phylogenetics and evolution in R languageCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1eitg%3D%3D&md5=510b6d28fb564dd94c49ca82a26c3899CAS |
[86] H. Wickham, The split-apply-combine strategy for data analysis J. Stat. Softw. 2011, 40, 1.
| The split-apply-combine strategy for data analysisCrossref | GoogleScholarGoogle Scholar |
[87] F. Kemp, Modern applied statistics with S Statistician 2003, 52, 704.
| Modern applied statistics with SCrossref | GoogleScholarGoogle Scholar |
[88] J. Oksanen, F.G. Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B. O’Hara, G.L. Simpson, P. Solymos, M.H.H. Stevens, H. Wagner, vegan: Community Ecology Package. R Package Version 2.0–10.2013 2015.
[89] C. Baker-Austin, M. Dopson, Life in acid: pH homeostasis in acidophiles Trends Microbiol. 2007, 15, 165.
| Life in acid: pH homeostasis in acidophilesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGisrw%3D&md5=6e51af8a42a272600e4aeda5058fb46aCAS |
[90] M. E. Trujillo, K. Hong, O. Genilloud, Family Micromonosporaceae, in The Prokaryotes 2014, pp. 499–569 (Springer: Berlin).
[91] A. Söllinger, C. Schwab, T. Weinmaier, A. Loy, A. T. Tveit, C. Schleper, T. Urich, Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences FEMS Microbiol. Ecol. 2016, 92, fiv149.
| Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferencesCrossref | GoogleScholarGoogle Scholar |
[92] D. Emerson, J. A. Rentz, T. G. Lilburn, R. E. Davis, H. Aldrich, C. Chan, C. L. Moyer, A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities PLoS One 2007, 2, e667.
| A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communitiesCrossref | GoogleScholarGoogle Scholar |
[93] W. Ghosh, B. Dam, Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea FEMS Microbiol. Rev. 2009, 33, 999.
| Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaeaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlShurrF&md5=18a0d4db0cf625e5fea95c002dc7e8b7CAS |
[94] G. S. Drysdale, G. H. Fleet, Acetic acid bacteria in winemaking: a review Am. J. Enol. Vitic. 2004, 39, 1.
[95] A. Sukenik, R. N. Kaplan-Levy, J. M. Welch, A. F. Post, Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria) ISME J. 2012, 6, 670.
| Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria)Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisVGgtrw%3D&md5=f53a320c8093e03cdd6b9e47a8de8ee8CAS |
[96] B. J. Campbell, L. Yu, J. F. Heidelberg, D. L. Kirchman, Activity of abundant and rare bacteria in a coastal ocean Proc. Natl. Acad. Sci. USA 2011, 108, 12776.
| Activity of abundant and rare bacteria in a coastal oceanCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVenu7bL&md5=88fe8b9afc928e3c39b32b69283782a8CAS |
[97] R. A. Edwards, B. Rodriguez-Brito, L. Wegley, M. Haynes, M. Breitbart, D. M. Peterson, M. O. Saar, S. Alexander, E. C. Alexander, F. Rohwer, Using pyrosequencing to shed light on deep mine microbial ecology BMC Genomics 2006, 7, 57.
| Using pyrosequencing to shed light on deep mine microbial ecologyCrossref | GoogleScholarGoogle Scholar |
[98] J. S. Brantner, Z. J. Haake, J. E. Burwick, C. M. Menge, S. T. Hotchkiss, J. M. Senko, Depth-dependent geochemical and microbiological gradients in Fe(III) deposits resulting from coal mine-derived acid mine drainage Front. Microbiol. 2014, 5, 215.
| Depth-dependent geochemical and microbiological gradients in Fe(III) deposits resulting from coal mine-derived acid mine drainageCrossref | GoogleScholarGoogle Scholar |
[99] I. Kamika, M. N. B. Momba, Microbial diversity of Emalahleni mine water in South Africa and tolerance ability of the predominant organism to vanadium and nickel PLoS One 2014, 9, e86189.
| Microbial diversity of Emalahleni mine water in South Africa and tolerance ability of the predominant organism to vanadium and nickelCrossref | GoogleScholarGoogle Scholar |
[100] J.-L. Kuang, L.-N. Huang, L.-X. Chen, Z.-S. Hua, S.-J. Li, M. Hu, J. T. Li, W. S. Shu, Contemporary environmental variation determines microbial diversity patterns in acid mine drainage ISME J. 2013, 7, 1038.
| Contemporary environmental variation determines microbial diversity patterns in acid mine drainageCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXms1Wit7c%3D&md5=21e6e1e5ace63566df791bba8eed3cd0CAS |
[101] M. Fabisch, F. Beulig, D. M. Akob, K. Kusel, Surprising abundance of Gallionella-related iron oxidizers in creek sediments at pH 4.4 or at high heavy metal concentrations Front. Microbiol. 2013, 4, 390.
[102] J. A. Fuhrman, J. A. Cram, D. M. Needham, Marine microbial community dynamics and their ecological interpretation Nat. Rev. Microbiol. 2015, 13, 133.
| Marine microbial community dynamics and their ecological interpretationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitlSgsr8%3D&md5=bd683cf0f8c641ae87c3fefc776d3831CAS |
[103] H. Teeling, B. M. Fuchs, D. Becher, C. Klockow, A. Gardebrecht, C. M. Bennke, M. Kassabgy, S. Huang, A. J. Mann, J. Waldmann, M. Weber, Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom Science 2012, 336, 608.
| Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloomCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1Gntrw%3D&md5=19a0cdfe9c6479b32c24a3644e73be0aCAS |
[104] M. Chodak, M. Gołębiewski, J. Morawska-Płoskonka, K. Kuduk, M. Niklińska, Soil chemical properties affect the reaction of forest soil bacteria to drought and rewetting stress Ann. Microbiol. 2015, 65, 1627.
| Soil chemical properties affect the reaction of forest soil bacteria to drought and rewetting stressCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitValsrjE&md5=073c4500da691b55b09827d6251a772fCAS |
[105] H.-S. Bae, M. E. Holmes, J. P. Chanton, K. R. Reddy, A. Ogram, Distribution, activities, and interactions of methanogens and sulfate-reducing prokaryotes in the Florida Everglades Appl. Environ. Microbiol. 2015, 81, 7431.
| Distribution, activities, and interactions of methanogens and sulfate-reducing prokaryotes in the Florida EvergladesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisFyrtro%3D&md5=db566f88580a77360c4d834464e13d32CAS |
