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Advances in the aquatic sciences
RESEARCH ARTICLE

Persistence, loss and appearance of bacteria upstream and downstream of a river system

Lisa M. Dann A E , Renee J. Smith A , Thomas C. Jeffries B , Jody C. McKerral C , Peter G. Fairweather A , Rod L. Oliver D and James G. Mitchell A
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Flinders University, Bedford Park, SA 5042, Australia.

B Hawkesbury Institute for the Environment. The University of Western Sydney, Richmond, NSW 2753, Australia.

C School of Computer Science, Engineering and Mathematics, Flinders University, Bedford Park, SA 5042, Australia.

D CSIRO Land and Water, Waite Research Institute, Urrbrae, SA 5064, Australia.

E Corresponding author. Email: lisa.dann@flinders.edu.au

Marine and Freshwater Research 68(5) 851-862 https://doi.org/10.1071/MF16010
Submitted: 11 January 2016  Accepted: 18 April 2016   Published: 12 July 2016

Abstract

Bacterial taxa shape microbial community composition and influence aquatic ecosystem dynamics. Studies on bacterial persistence in rivers have primarily focussed on microbial-source tracking as an indicator for faecal-source contamination, whereas archetypal freshwater species have received minimal attention. The present study describes the river microbial communities upstream and 3.3 km downstream of a small rural town. By 16S rDNA sequencing, we report three patterns in microbial community composition, namely, persistence, loss and appearance. Persistence was observed as 46% inter-site similarity, perhaps owing to generalists that have information lengths that exceed 3.3 km and are capable of adapting to system fluctuations. Loss was observed as 10% site exclusivity upstream, perhaps owing to removal processes such as predation and lysis during transport downstream. Last, appearance was observed as 44% site exclusivity downstream, indicating potential anthropogenic impacts from land run-off on bacterial community composition. High multivariate dispersion among downstream samples, as well as overall sample dissimilarity, present as microscale hotspots of discrete Firmicutes and Cyanobacteria species, indicated higher heterogeneity downstream, and therefore increased patchiness from downstream transport and inputs of bacterial genotypes. These findings suggest relativities among three fates for bacterial species of fluvial systems, persistence, loss and appearance, with each having different effects on system dynamics.

Additional keywords: bacterioplankton, dispersal, diversity, freshwater, Murray–Darling system, running water, water column.


References

Adams, H. E., Crump, B. C., and Kling, G. W. (2014). Metacommunity dynamics of bacteria in an arctic lake: the impact of species sorting and mass effects on bacterial production and biogeography. Frontiers in Microbiology 5, 1–10.
Metacommunity dynamics of bacteria in an arctic lake: the impact of species sorting and mass effects on bacterial production and biogeography.Crossref | GoogleScholarGoogle Scholar |

Alauzet, C., Marchandin, H., Courtin, P., Mory, F., Lemée, L., Pons, J. L., Chapot-Chartier, M. P., Lozniewski, A., and Jumas-Bilak, E. (2014). Multilocus analysis reveals diversity in the genus Tissierella: description of Tissierella carlieri sp. nov. in the new class Tissierellia classis nov. Systematic and Applied Microbiology 37, 23–34.
Multilocus analysis reveals diversity in the genus Tissierella: description of Tissierella carlieri sp. nov. in the new class Tissierellia classis nov.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVagtrjN&md5=bf62d312fc3cfd09a8b7f6ac51218fb4CAS | 24268443PubMed |

Anderson, M. J., Gorley, R. N., and Clarke, K. R. (2008). Tests of homogeneity of dispersions (PERMDISP). In ‘PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods’. pp. 87–122. (PRIMER-E: Plymouth, UK.)

Andersson, A. F., Lindberg, M., Jakobsson, H., Bäckhed, F., Nyrén, P., and Engstrand, L. (2008). Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One 3, e2836.
Comparative analysis of human gut microbiota by barcoded pyrosequencing.Crossref | GoogleScholarGoogle Scholar | 18665274PubMed |

Azam, F. (1998). Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694–696.
Microbial control of oceanic carbon flux: the plot thickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtVOks7w%3D&md5=1a30a865db1acc737fdbbe80e1873334CAS |

Bassis, C. M., Tang, A. L., Young, V. B., and Pynnonen, M. A. (2014). The nasal cavity microbiota of healthy adults. Microbiome 2, 27.
The nasal cavity microbiota of healthy adults.Crossref | GoogleScholarGoogle Scholar | 25143824PubMed |

Bettarel, Y., Amblard, C., Sime-Ngando, T., Carrias, J. F., Sargos, D., Garabétian, F., and Lavandier, P. (2003). Viral lysis, flagellate grazing potential and bacterial production in Lake Pavin. Microbial Ecology 45, 119–127.
Viral lysis, flagellate grazing potential and bacterial production in Lake Pavin.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s7gsFyqtw%3D%3D&md5=6162ad51c9a44528e7e27b0afb565f8eCAS | 12545309PubMed |

Brown, M. V., Lauro, F. M., DeMaere, M. Z., Muir, L., Wilkins, D., Thomas, T., Riddle, M. J., Fuhrman, J. A., Andrews-Pfannkoch, C., Hoffman, J. M., McQuaid, J. B., Allen, A., Rintoul, S. R., and Cavicchioli, R. (2012). Global biogeography of SAR11 marine bacteria. Molecular Systems Biology 8, 1–13.
Global biogeography of SAR11 marine bacteria.Crossref | GoogleScholarGoogle Scholar |

Brussaard, C. (2004). Optimisation of procedures for counting viruses by flow cytometry. Applied and Environmental Microbiology 70, 1506–1513.
Optimisation of procedures for counting viruses by flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisVKju7k%3D&md5=479a44970a5f212aeccd1e4bb10aabceCAS | 15006772PubMed |

Brussaard, C., Marie, D., and Bratbak, G. (2000). Flow cytometric detection of viruses. Journal of Virological Methods 85, 175–182.
Flow cytometric detection of viruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVKksQ%3D%3D&md5=061f3d448317735e5dada5f0e6569492CAS | 10716350PubMed |

Caporaso, G. J., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Gonzalez Peña, A., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J., and Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.
QIIME allows analysis of high-throughput community sequencing data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFalurg%3D&md5=70359596b4284c2a688a79bdb1c415fdCAS |

Chow, C. E. T., Kim, D. Y., Sachdeva, R., Caron, D. A., and Fuhrman, J. A. (2014). Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. The International Society for Microbial Ecology Journal 8, 816–829.
| 1:CAS:528:DC%2BC2cXkslGqs7Y%3D&md5=d72954262c4c7034adb2f4ceda51f798CAS |

Clarke, K. R., and Gorley, R. N. (2014). Contributions of variables to similarity (SIMPER). In ‘PRIMER v7: User Manual/tutorial’. pp. 140–142. (PRIMER-E: Plymouth, UK.)

Clarke, K. R., and Warwick, R. M. (2001) Hierarchical clustering. In ‘Change in Marine Communities: an Approach to Statistical Analysis and Interpretation’. pp. 1–3. (PRIMER-E: Plymouth, UK.)

Clauset, A., Shalizi, C. R., and Newman, M. E. J. (2009). Power-law distributions in empirical data. Society for Industrial and Applied Mathematics Review 51, 661–703.

Cook, P. G., Leaney, F. W., and Jolly, I. D. (2001). Groundwater recharge in the Mallee Region, and salinity implications for the Murray River – a review. CSIRO technical report 45/01, CSIRO Land and Water. Available at http://www.clw.csiro.au/publications/technical2001/tr45-01.pdf [Verified 26 May 2016].

Crump, B. C., Kling, G. W., Bahr, M., and Hobbie, J. E. (2003). Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source. Applied and Environmental Microbiology 69, 2253–2268.
Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source.Crossref | GoogleScholarGoogle Scholar | 12676708PubMed |

Dann, L. M., Mitchell, J. G., Speck, P. G., Newton, K., Jeffries, T., and Paterson, J. (2014). Virio- and bacterioplankton distributions at the sediment–water interface. PLOS One 9, e102805.
Virio- and bacterioplankton distributions at the sediment–water interface.Crossref | GoogleScholarGoogle Scholar | 25057797PubMed |

Dann, L. M., Paterson, J. S., Newton, K., Oliver, R., and Mitchell, J. G. (2016). Distributions of virus-like particles and prokaryotes within microenvironments. PLOS One 11, e0146984.
Distributions of virus-like particles and prokaryotes within microenvironments.Crossref | GoogleScholarGoogle Scholar | 26785114PubMed |

de Menezes, A. B., Lewis, E., O’Donovan, M., O’Neill, B. F., Clipson, N., and Doyle, E. M. (2011). Microbiome analysis of dairy cows fed pasture or total mixed ration diets. FEMS Microbial Ecology 78, 256–265.
Microbiome analysis of dairy cows fed pasture or total mixed ration diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCksrjP&md5=b37f447154e70a7f61c7ceeea68056c8CAS |

DEWNR (2014). River Murray flow report. Public I2 A2. Department of Environment Water and Natural Resources, Government of South Australia, Adelaide, SA.

Duarte, C. M., and Vaque, D. (1992). Scale dependence of bacterioplankton patchiness. Marine Ecology Progress Series 84, 95–100.

Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Search and clustering orders of magnitude faster than BLAST.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1WhtbzM&md5=fe304dcc37de187a309c2879cf36e5d2CAS | 20709691PubMed |

Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998.
UPARSE: highly accurate OTU sequences from microbial amplicon reads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1ylsLzE&md5=e15a1e38f4611d0e16a5c0bbec2c0e49CAS | 23955772PubMed |

Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.
UCHIME improves sensitivity and speed of chimera detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVSiurvL&md5=2588fa1a0689d1c108d0df4282cfd9e4CAS | 21700674PubMed |

Edwards, R. A., and Rohwer, F. (2005). Viral metagenomics. Nature Reviews. Microbiology 3, 504–510.
Viral metagenomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksFKmsLs%3D&md5=8682ca48f8f1c0d0b5abb29849bd3a73CAS | 15886693PubMed |

Eleria, A., and Vogel, R. M. (2005). Prediciting faecal coliform bacteria levels in the Charles River, Massachusetts, USA. Journal of the American Water Resources Association 41, 1195–1209.
Prediciting faecal coliform bacteria levels in the Charles River, Massachusetts, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtF2nu7vP&md5=c891daf379a3e1cb6cf199be25beb13cCAS |

Finlay, B. J., Maberly, S. C., and Cooper, J. I. (1997). Microbial diversity and ecosystem function. Oikos Journal 80, 209–213.
Microbial diversity and ecosystem function.Crossref | GoogleScholarGoogle Scholar |

Fries, J., Characklis, G., and Noble, R. (2006). Attachment of faecal indicator bacteria to particles in the Neuse River estuary, NC. Journal of Environmental Engineering 132, 1338–1345.
Attachment of faecal indicator bacteria to particles in the Neuse River estuary, NC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsFyjsbY%3D&md5=726551338451184794db14f35fde661dCAS |

Fries, J. S., Characklis, G. W., and Noble, R. T. (2008). Sediment-water exchange of Vibrio sp. and faecal indicator bacteria: implications for persistence and transport in the Neuse River estuary, North Carolina, USA. Water Research 42, 941–950.
Sediment-water exchange of Vibrio sp. and faecal indicator bacteria: implications for persistence and transport in the Neuse River estuary, North Carolina, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvFyrurw%3D&md5=8572073cd52566f7b6294643aba141aaCAS | 17945328PubMed |

Goss, K. F. (2003). Environmental flows, river salinity and biodiversity conservation: managing trade-offs in the Murray–Darling Basin. Australian Journal of Botany 51, 619–625.
Environmental flows, river salinity and biodiversity conservation: managing trade-offs in the Murray–Darling Basin.Crossref | GoogleScholarGoogle Scholar |

Hahn, M. W., and Höfle, M. G. (1999). Flagellate predation on a bacterial model community: interplay of size-selective grazing, specific bacterial cell size and bacterial community composition. Applied and Environmental Microbiology 65, 4863–4872.
| 1:CAS:528:DyaK1MXnt1WmtLc%3D&md5=14c5f470274cac6cfcaab33a40520377CAS | 10543797PubMed |

Hoffmann, K. H., Rodriguez-Brito, B., Breitbart, M., Bangor, D., Angly, F., Felts, B., Nulton, J., Rohwer, F., and Salamon, P. (2007). Power law rank-abundance models for marine phage communities. FEMS Microbiology Letters 273, 224–228.
Power law rank-abundance models for marine phage communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFarurg%3D&md5=600a7d53e9254b314e721b470d175034CAS | 17559407PubMed |

Jones, S. E., Newton, R. J., and McMahon, K. D. (2008). Potential for atmospheric deposition of bacteria to influence bacterioplankton communities. FEMS Microbiology Ecology 64, 388–394.
Potential for atmospheric deposition of bacteria to influence bacterioplankton communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFajtLY%3D&md5=459ba7b68870e2ab7287b6ff66e55460CAS | 18393990PubMed |

Karr, J. R., and Chu, E. W. (2000). Sustaining living rivers. Hydrobiologia 422/423, 1–14.
Sustaining living rivers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVamsrs%3D&md5=c50a5ee6cc0bc78d709ac5cbe6ef0efcCAS |

Kiem, A. S., and Verdon-Kidd, D. C. (2011). Steps toward ‘useful’ hydroclimatic scenarios for water resource management in the Murray–Darling Basin. Water Resources Research 47, W00G06.
Steps toward ‘useful’ hydroclimatic scenarios for water resource management in the Murray–Darling Basin.Crossref | GoogleScholarGoogle Scholar |

Konopka, A. (2009). What is microbial community ecology? The International Society for Microbial Ecology Journal 3, 1223–1230.

Leff, L. G., McArthur, J. V., and Shimkets, L. J. (1992). Information spiralling: movement of bacteria and their genes in streams. Microbial Ecology 24, 11–24.
Information spiralling: movement of bacteria and their genes in streams.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7jtlSjsQ%3D%3D&md5=f460cbae76c7ae9eb4e6db0c86ab0cd8CAS | 24193036PubMed |

Liu, A. C., Chou, C. Y., Chen, L. L., and Kuo, C. H. (2015). Bacterial community dynamics in a swine wastewater anaerobic reactor revealed by 16S rDNA sequence analysis. Journal of Biotechnology 194, 124–131.
Bacterial community dynamics in a swine wastewater anaerobic reactor revealed by 16S rDNA sequence analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXltVahtw%3D%3D&md5=ef172ff62c28f7b984b361f86ab5ec31CAS | 25500375PubMed |

Long, R. A., and Azam, F. (2001). Microscale patchiness of bacterioplankton assemblage richness in seawater. Aquatic Microbial Ecology 26, 103–113.
Microscale patchiness of bacterioplankton assemblage richness in seawater.Crossref | GoogleScholarGoogle Scholar |

Marie, D., Partensky, F., Jacquet, S., and Vaulot, D. (1997). Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Applied and Environmental Microbiology 63, 186–193.
| 1:CAS:528:DyaK2sXhs1Oiug%3D%3D&md5=ee7df4bf3fb11d1c92f4bb989da52d9cCAS | 16535483PubMed |

Marie, D., Brussaard, C., Thyrhaug, R., Bratbak, G., and Vauolt, D. (1999). Enumeration of marine viruses in culture and natural samples by flow cytometry. Applied and Environmental Microbiology 65, 45–52.
| 1:CAS:528:DyaK1MXjvVyisA%3D%3D&md5=4c56ca39f7c16d96f1f72a2853224b9bCAS | 9872758PubMed |

McArthur, J. V., and Tuckfield, R. C. (1997). Information length: spatial and temporal parameters among stream bacterial assemblages. Journal of the North American Benthological Society 16, 347–357.
Information length: spatial and temporal parameters among stream bacterial assemblages.Crossref | GoogleScholarGoogle Scholar |

McArthur, J. V., Leff, L. G., and Smith, M. H. (1992). Genetic diversity of bacteria along a stream continuum. Journal of the North American Benthological Society 11, 269–277.
Genetic diversity of bacteria along a stream continuum.Crossref | GoogleScholarGoogle Scholar |

Meehan, C. J., and Beiko, R. G. (2014). A phylogenomic view of ecological specialisation in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biology and Evolution 6, 703–713.
A phylogenomic view of ecological specialisation in the Lachnospiraceae, a family of digestive tract-associated bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtlWrtbo%3D&md5=1eed2ed45a27f09f2f8d5ff63b6022e1CAS | 24625961PubMed |

Meyer, J. L. (1994). The microbial loop in flowing waters. Microbial Ecology 28, 195–199.
The microbial loop in flowing waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1Wktb8%3D&md5=4e1d881d28d1b76fbcf674a20b475272CAS | 24186445PubMed |

Mitchell, J. G., and Fuhrman, J. A. (1989). Centimetre scale vertical heterogeneity in bacteria and chlorophyll a. Marine Ecology Progress Series 54, 141–148.
Centimetre scale vertical heterogeneity in bacteria and chlorophyll a.Crossref | GoogleScholarGoogle Scholar |

Moore, G. F., Dunsmore, B. C., Jones, S. M., Smejkal, C. W., Jass, J., Stoodley, P., and Lappin-Scott, H. M. (2000). Microbial detachment from biofilms. In ‘Community Structure and Co-operation in Biofilms. Society for General Microbiology Symposia (Number 59)’. (Eds D. G Allison, P. Gilbert, H. M Lappin-Scott, and M. Wilson.) pp. 107–128. (Cambridge University Press: Cambridge, UK.)10.1017/CBO9780511754814

Newbold, J. D., Elwood, J. W., O’Neil, R. V., and Van Winkle, W. (1981). Measuring nutrient spiralling in streams. Canadian Journal of Fisheries and Aquatic Sciences 38, 860–863.
Measuring nutrient spiralling in streams.Crossref | GoogleScholarGoogle Scholar |

Newbold, J. D., Elwood, J. W., O’Neill, R. V., and Sheldon, A. L. (1983). Phosphorus dynamics in a woodland stream ecosystem: a study of nutrient spiralling. Ecology 64, 1249–1265.
Phosphorus dynamics in a woodland stream ecosystem: a study of nutrient spiralling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXmtVSitb0%3D&md5=7c06fb4415d478ffbc281872f35ec55fCAS |

Newton, R. J., Kent, A. D., Triplett, E. W., and McMahon, K. D. (2006). Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes. Environmental Microbiology 8, 956–970.
Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes.Crossref | GoogleScholarGoogle Scholar | 16689717PubMed |

Newton, R. J., Jones, S. E., Helmus, M. R., and McMahon, K. D. (2007). Phylogenetic ecology of the freshwater Actinobacteria acI lineage. Applied and Environmental Microbiology 73, 7169–7176.
Phylogenetic ecology of the freshwater Actinobacteria acI lineage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFyjsA%3D%3D&md5=f1083097ee0e93f99cc294b87522afc7CAS | 17827330PubMed |

Pylro, V. S., Roesch, L. F. W., Morais, D. K., Clark, I. M., Hirsch, P. R., and Tótola, M. R. (2014). Data analysis for 16S microbial profiling from different benchtop sequencing platforms. Journal of Microbiological Methods 107, 30–37.
Data analysis for 16S microbial profiling from different benchtop sequencing platforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFagt7zF&md5=b387ecd72cda4e7f3ccf8e06a2501fb2CAS | 25193439PubMed |

Rodriguez-Brito, B., Li, L., Wegley, L., Furlan, M., Angly, F., Breitbart, M., Buchanan, J., Desnues, C., Dinsdale, L., Edwards, R., Felts, B., Haynes, M., Liu, H., Lipson, D., Mahaffy, J., Martin-Cuadrado, A. B., Mira, A., Nulton, J., Pašić, L., Rayhawk, S., Rodriguez-Mueller, J., Rodriguez-Valera, F., Salamon, P., Srinagesh, S., Thingstad, T. F., Tran, T., Vega Thurber, R., Willner, D., Youle, M., and Rohwer, F. (2010). Viral and microbial community dynamics in four aquatic environments. The International Society for Microbial Ecology Journal 4, 739–751.

Rodriguez-Valera, F., Martin-Cuadrado, A. B., Rodriguez-Brito, B., Pašić, L., Thingstad, T. F., Rohwer, F., and Mira, A. (2009). Explaining microbial population genomics through phage predation. Nature Reviews. Microbiology 7, 828–836.
Explaining microbial population genomics through phage predation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Kqsb7K&md5=089a7d91324436a6c1ec2ee9d1071de1CAS | 19834481PubMed |

Roudnew, B., Seymour, J. R., Jeffries, T. C., Lavery, T. J., Smith, R. J., and Mitchell, J. G. (2012). Bacterial and virus-like particle abundances in purged and unpurged groundwater depth profiles. Ground Water Monitoring and Remediation 32, 72–77.
Bacterial and virus-like particle abundances in purged and unpurged groundwater depth profiles.Crossref | GoogleScholarGoogle Scholar |

Roudnew, B., Lavery, T. J., Seymour, J. R., Jeffries, T. C., and Mitchell, J. G. (2014). Variability in bacteria and virus-like particle abundances during purging of unconfined aquifers. Ground Water 52, 118–124.
Variability in bacteria and virus-like particle abundances during purging of unconfined aquifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXislOqsQ%3D%3D&md5=8e03667246d329f77f60280042606775CAS | 23550819PubMed |

Sax, D. F., Stachowicz, J. J., Brown, J. H., Bruno, J. F., Dawson, M. N., Gaines, S. D., Grosberg, R. K., Hastings, A., Holt, R. D., Mayfield, M. M., O’Connor, M. I., and Rice, W. R. (2007). Ecological and evolutionary insights from species invasions. Trends in Ecology & Evolution 22, 465–471.
Ecological and evolutionary insights from species invasions.Crossref | GoogleScholarGoogle Scholar |

Seymour, J. R., and Stocker, R. (2009). Resource patch formation and exploitation throughout the marine microbial food web. American Naturalist 173, E15–E29.
Resource patch formation and exploitation throughout the marine microbial food web.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FitlCntQ%3D%3D&md5=e0e91c9a784b4c42e7065491f802ddaeCAS | 19053839PubMed |

Seymour, J. R., Mitchell, J. G., Pearson, L., and Waters, R. (2000). Heterogeneity in bacterioplankton abundance from 4.5 millimetre resolution sampling. Aquatic Microbial Ecology 22, 143–153.
Heterogeneity in bacterioplankton abundance from 4.5 millimetre resolution sampling.Crossref | GoogleScholarGoogle Scholar |

Seymour, J. R., Mitchell, J. G., and Seuront, L. (2004). Microscale heterogeneity in the activity of coastal bacterioplankton communities. Aquatic Microbial Ecology 35, 1–16.
Microscale heterogeneity in the activity of coastal bacterioplankton communities.Crossref | GoogleScholarGoogle Scholar |

Seymour, J. R., Seuront, L., and Mitchell, J. G. (2005). Microscale and small-scale temporal dynamics of a coastal planktonic microbial community. Marine Ecology Progress Series 300, 21–37.
Microscale and small-scale temporal dynamics of a coastal planktonic microbial community.Crossref | GoogleScholarGoogle Scholar |

Seymour, J. R., Seuront, L., and Mitchell, J. G. (2007). Microscale gradients of planktonic microbial communities above the sediment surface in a mangrove estuary. Estuarine, Coastal and Shelf Science 73, 651–666.
Microscale gradients of planktonic microbial communities above the sediment surface in a mangrove estuary.Crossref | GoogleScholarGoogle Scholar |

Simberloff, D. (1978). Use of rarefaction and related methods in ecology. In ‘Biological Data in Water Pollution Assessment: Quantitative and Statistical Analyses’. (Eds K. L. Dickson and J. Cairns Jr.) pp. 150–165. (American Society for Testing and Materials: Philadelphia, PA.)

Smith, R. J., Paterson, J. S., Sibley, C. A., Hutson, J. L., and Mitchell, J. G. (2015). Putative effect of aquifer recharge on the abundance and taxonomic composition of endemic microbial communities. PLOS One 10, e0129004.
Putative effect of aquifer recharge on the abundance and taxonomic composition of endemic microbial communities.Crossref | GoogleScholarGoogle Scholar | 26083532PubMed |

Stackebrandt, E., Cummins, C. S., and Johnson, J. L. (2006). Family Propionibacteriaeceae: the genus Propionibacterium. In ‘The Prokaryotes’. (Eds M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt.) pp. 400–418. (Springer: New York.)

Stocker, R. (2012). Marine microbes see a sea of gradients. Science 338, 628–633.
Marine microbes see a sea of gradients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFygtbvE&md5=7470391933834488b70b7d14740a1acdCAS | 23118182PubMed |

Stocker, R., Seymour, J. R., Samadani, A., Hunt, D. E., and Polz, M. F. (2008). Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proceedings of the National Academy of Sciences of the United States of America 105, 4209–4214.
Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkt1Wkt70%3D&md5=5e1e32894f726dcd07e16383d21dc0afCAS | 18337491PubMed |

Teneva, I., Dzhambazov, B., Koleva, L., Mladenov, R., and Schirmer, K. (2005). Toxic potential of five freshwater Phormidium species (Cyanoprokaryota). Toxicon 45, 711–725.
Toxic potential of five freshwater Phormidium species (Cyanoprokaryota).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVSgtrg%3D&md5=7938cea525e3f205720d61c909217f49CAS | 15804520PubMed |

Thingstad, F. T. (2000). Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnology and Oceanography 45, 1320–1328.
Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems.Crossref | GoogleScholarGoogle Scholar |

Thingstad, F. T., and Lignell, R. (1997). Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology 13, 19–27.
Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand.Crossref | GoogleScholarGoogle Scholar |

Tonon, L. A. C., Moreira, A. P. B., and Thompson, F. (2014). The family Erythrobacteraceae. In ‘The Prokaryotes: Alphaproteobacteria and Betaproteobacteria’. (Eds E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, and F Thompson.) pp. 213–235 (Springer-Verlag: Heidelberg, Germany.)

Traister, E., and Anisfeld, S. C. (2006). Variability of indicator bacteria at different time scales in the upper Hoosic River watershed. Environmental Science & Technology 40, 4990–4995.
Variability of indicator bacteria at different time scales in the upper Hoosic River watershed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntVKgsLc%3D&md5=a9b89f82bedc33b913a65378cbc49633CAS |

Van der Gucht, K., Cottenie, K., Muylaert, K., Vloemans, N., Cousin, S., Declerck, S., Jeppesen, E. J. M., Schwenk, K., Zwart, G., Degans, H., Vyverman, W., and De Meester, L. (2007). The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proceedings of the National Academy of Sciences of the United States of America 104, 20404–20409.
The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjslenuw%3D%3D&md5=51880afb49504e8055f8c3c9b62ec2bcCAS | 18077371PubMed |

van Dijk, A. I. J. M., Hairsine, P. B., Arancibia, J. P., and Dowling, T. I. (2007). Reforestation, water availability and stream salinity: a multi-scale analysis in the Murray–Darling Basin, Australia. Forest Ecology and Management 251, 94–109.
Reforestation, water availability and stream salinity: a multi-scale analysis in the Murray–Darling Basin, Australia.Crossref | GoogleScholarGoogle Scholar |

Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267.
Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsleqtrc%3D&md5=5136270b6f73eeddd731483262ce6233CAS | 17586664PubMed |

Wang, Y., Sheng, H. F., He, Y., Wu, J. Y., Jiang, Y. X., Tam, N. F. Y., and Zhou, H. W. (2012). Comparison of the levels of bacterial diversity in freshwater, intertidal wetland and marine sediments by using millions of Illumina tags. Applied and Environmental Microbiology 78, 8264–8271.
Comparison of the levels of bacterial diversity in freshwater, intertidal wetland and marine sediments by using millions of Illumina tags.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1yktrrF&md5=bbab8f419d58ba89af8379b863769b30CAS | 23001654PubMed |

Warnecke, F., Amann, R., and Pernthaler, J. (2004). Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environmental Microbiology 6, 242–253.
Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitlOhtbc%3D&md5=5ecfa628035d10d027436166a1fdeccfCAS | 14871208PubMed |

Webster, J. R., and Patten, B. C. (1979). Effects of watershed perturbation on stream potassium and calcium dynamics. Ecological Monographs 49, 51–72.
Effects of watershed perturbation on stream potassium and calcium dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlt1yksbY%3D&md5=5ea1d2b4186daa0ce46b54c0eb3ba94aCAS |

Weinbauer, M. G., and Höfle, M. G. (1998). Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Applied and Environmental Microbiology 64, 431–438.
| 1:CAS:528:DyaK1cXpsVSltg%3D%3D&md5=0e40fc9731c7a9e30af658f416c43207CAS | 16349497PubMed |

Weinbauer, M. G., Hornák, K., Jezbera, J., Nedoma, J., Dolan, J. R., and Šimek, K. (2007). Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity. Environmental Microbiology 9, 777–788.
Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1GmsLY%3D&md5=b2a9ac29366dec7565c1ffeadf2f8a97CAS | 17298376PubMed |

Wiese, J., Thiel, V., Gärtner, A., Schmaljohann, R., and Imhoff, J. F. (2009). Kiloniella laminariae gen. nov., sp. nov., an alphaproteobacterium from the marine macroalga Laminaria saccharina. International Journal of Systematic and Evolutionary Microbiology 59, 350–356.
Kiloniella laminariae gen. nov., sp. nov., an alphaproteobacterium from the marine macroalga Laminaria saccharina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslalsLc%3D&md5=d63789a425b0a6e17c5f20a8983ad997CAS | 19196777PubMed |

Winter, C., Bouvier, T., Weinbauer, M. G., and Thingstad, T. F. (2010). Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner’ hypothesis revisited. Microbiology and Molecular Biology Reviews 74, 42–57.
Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner’ hypothesis revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFOlu7Y%3D&md5=5a05e5d51b026d49c261921606ad7477CAS | 20197498PubMed |

Wise, M. G., Shimkets, L. J., and McArthur, J. V. (1995). Genetic structure of a lotic population of Burkholderia (Pseudomonas) cepacia. Applied and Environmental Microbiology 61, 1791–1798.
| 1:CAS:528:DyaK2MXlsFyktrY%3D&md5=13e0a680c41edee5f5930a39a3e4c91fCAS | 7646017PubMed |

Wu, X., Xi, W., Ye, W., and Yang, H. (2007). Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiology Ecology 61, 85–96.
Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVags74%3D&md5=14ff334b241469361840fd8ddd9e18d0CAS | 17506827PubMed |

Zwart, G., Crump, B. C., Agterveld, M. P. K., Hagen, F., and Han, S. K. (2002). Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquatic Microbial Ecology 28, 141–155.
Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers.Crossref | GoogleScholarGoogle Scholar |