Cite this paper:
Kelly NEWTON, Thomas C. JEFFRIES, Renee J. SMITH, Justin R. SEYMOUR, Laurent SEURONT, James G. MITCHELL. Taxonomic and metabolic shifts in the Coorong bacterial metagenome driven by salinity and external inputs[J]. HaiyangYuHuZhao, 2018, 36(6): 2033-2049

Taxonomic and metabolic shifts in the Coorong bacterial metagenome driven by salinity and external inputs

Kelly NEWTON1, Thomas C. JEFFRIES1,2, Renee J. SMITH1,3, Justin R. SEYMOUR1,4, Laurent SEURONT1,5, James G. MITCHELL1
1 School of Biological Sciences, Flinders University, PO Box 2100, Bedford Park, SA 5042, Australia;
2 School of Science and Health, Western Sydney University, Richmond NSW 2753, Australia;
3 Flinders Centre for Innovation in Cancer, Flinders University, Bedford Park, SA 5042, Australia;
4 Climate Change Cluster, University of Technology Sydney, Sydney NSW 2007, Australia;
5 Centre National de la Recherche Scientifique, Laboratoire d'Océanologie et de Géosciences, CNRS UMR 8187 LOG, Wimereux, France
The Coorong estuary lies at the terminus of Australia's largest river system, the Murray-Darling; both are strongly influenced by human activities; including farming and extensive flow modification. Metagenomic approaches were used to determine the planktonic bacterial community composition and potential metabolic function at two extremes in the Coorong, the river mouth which exhibits marine-like salinity, and the hypersaline upper-reaches of the estuary. Significant shifts in taxa and metabolic function were seen between the two sites. The river mouth exhibited an increase in abundance of Rhodobacteriaceae and Alteromonadaceae; families readily able to adapt to change in nutrient conditions; and the potentially pathogenic families Brucellaceae, Enterobacteriaceae and Vibrionaceae. Metabolisms over-represented include motility and chemotaxis, RNA metabolism and membrane transport, all of which are involved in actively searching for and obtaining nutrients. Also over-represented were metabolisms involved in population succession and stress response. An over-representation of taxa and metabolisms indicative of environmental change is reflective of anthropogenically affected riverine input. In the hypersaline upper reaches of the estuary, the halophilic family Ectothiorhodospiraceae was over-represented, as were the families Flavobacteriaceae, Cytophagaceae and Nocardioidaceae, members of which are able to survive over a wide salinity range. Metabolisms over-represented here were reflective of increased bacterial growth, characteristic of hypersaline environments, and included DNA metabolism, nucleotide and nucleoside synthesis and cell cycle. Coorong metagenomes clustered taxonomically and metabolically with other planktonic metagenomes, but remained an outlier of this group with only 71% and 84% similarity, respectively. This indicates that the Coorong exhibits a unique planktonic bacterial community that is influenced by riverine input at the river mouth and salinity in the upper-reaches.
Key words:    hypersaline|estuary|bacteria|taxonomy|metabolic potential   
Received: 2017-12-21   Revised:
PDF (621 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by Kelly NEWTON
Articles by Thomas C. JEFFRIES
Articles by Renee J. SMITH
Articles by Justin R. SEYMOUR
Articles by Laurent SEURONT
Articles by James G. MITCHELL
Allers E, Gómez-Consarnau L, Pinhassi J, Gasol J M, Šimek K, Pernthaler J. 2007. Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ. Microbiol., 9(10):2 417-2 429.
Alonso-Sáez L, Arístegui J, Pinhassi J, Gómez-Consarnau L, González J M, Vaqué D, Agustí S, Gasol J M. 2007.Bacterial assemblage structure and carbon metabolism along a productivity gradient in the NE Atlantic Ocean.Aquat. Microb. Ecol., 46(1):43-53.
Ayub N D, Pettinari M J, Ruiz J A, López N I. 2004. A polyhydroxybutyrate-producing Pseudomonas sp.Isolated from Antarctic environments with high stress resistance. Curr. Microbiol., 49(3):170-174.
Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol., 5(10):782-791.
Barillé-Boyer A L, Barillé L, Massé H, Razet D, Héral M. 2003. Correction for particulate organic matter as estimated by loss on ignition in estuarine ecosystems.Estuar. Coast. Shelf Sci., 58(1):147-153.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate:a practical and powerful approach to multiple testing.J. Roy. Statist. Soc. Ser. B., 57(1):289-300.
Benlloch S, López-López A, Casamayor E O, Øvreås L, Goddard V, Daae F L, Smerdon G, Massana R, Joint I, Thingstad F, Pedrós-Alió C, Rodríguez-Valera F. 2002.Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ. Microbiol., 4(6):349-360.
Biers E J, Sun S L, Howard E C. 2009. Prokaryotic genomes and diversity in surface ocean waters:Interrogating the Global Ocean Sampling metagenome. Appl. Environ.Microbiol., 75(7):2 221-2 229.
Blackburn N, Fenchel T, Mitchell J G. 1998. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science, 282(5397):2 254-2 256.
Bouvier T C, del Giorgio P A. 2002. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol. Oceanogr., 47(2):453-470.
Bowman J P, Nichols D S. 2005. Novel members of the family Flavobacteriaceae from Antarctic maritime habitats including Subsaximicrobium wynnwilliamsii gen. nov., sp. nov., Subsaximicrobium saxinquilinus sp. nov., Subsaxibacter broadyi gen. nov., sp. nov., Lacinutrix copepodicola gen. nov., sp. nov., and novel species of the genera Bizionia, Gelidibacter and Gillisia. Int. J. Syst.Evol. Microbiol., 55(4):1 471-1 486.
Brindefalk B, Ettema T J G, Viklund J, Thollesson M, Andersson S G E. 2011. A phylometagenomic exploration of oceanic Alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS One, 6(9):e24457.
Brussaard C P D. 2004. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ.Microbiol., 70(3):1 506-1 513.
Bull A T, Stach J E M, Ward A C, Goodfellow M. 2005. Marine actinobacteria:perspectives, challenges, future directions.Antonie van Leeuwenhoek, 87(1):65-79.
Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int.Microbiol., 3(1):3-8.
Chapelle F H, Lovley D R. 1990. Rates of microbial metabolism in deep coastal plain aquifers. Appl. Environ. Microbiol., 56(6):1 865-1 874.
Clarke K R, Gorley R N. 2006. PRIMER v6:User Manual/Tutorial. PRIMER-E, Plymouth, UK.
Clarke K R. 1993. Non-parametric multivariate analyses of changes in community structure. Austr. J. Ecol., 18(1):117-143.
Cottrell M T, Waidner L A, Yu L Y, Kirchman D L. 2005.Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environ. Microbiol., 7(12):1 883-1 895.
Cugley J, Shukla C, Sarneckis K. 2002. Ambient Water Quality Monitoring of the River Murray 1990-1999 Report No.1.Environment Protection Agency South Australia, Adelaide. 103p.
DeLong E F, Preston C M, Mincer T, Rich V, Hallam S J, Frigaard N-U, Martinez A, Sullivan M B, Edwards R, Brito B R, Chisholm S W, Karl D M. 2006. Community genomics among stratified microbial assemblages in the ocean's interior. Science, 311(5760):496-503.
Dinsdale E A, Pantos O, Smriga S, Edwards R A, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin S A, Thurber R V, Willis B L, Azam F, Knowlton N, Rohwer F. 2008. Microbial ecology of four coral atolls in the Northern Line Islands. PLoS One, 3(2):e1584.
Dobson S J, Colwell R R, McMeekin T A, Franzmann P D. 1993. Direct sequencing of the polymerase chain reactionamplified 16S rRNA gene of Flavobacterium gondwanense sp. nov. and Flavobacterium salegens sp.nov., two new species from a hypersaline Antarctic lake.Int. J. Syst. Bacteriol., 43(1):77-83.
Edwards R A, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson D M, Saar M O, Alexander S, Alexander Jr E C, Rohwer F. 2006. Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics, 7:57.
Esteban J A, Salas M, Blanco L. 1993. Fidelity of ϕ29 DNA Polymerase. J. Biol. Chem., 268(4):2 719-2 726.
Fisher W D. 1958. On grouping for maximum homogeneity. J.Am. Statist. Assoc., 53(284):789-798.
Ford P W. 2007. Biogeochemistry of the Coorong. Review and identification of future research requirements. CSIRO Water for a Healthy Country National Research Flagship.CSIRO, Canberra. 23p.
Garrity G M, Bell J A, Lilburn T. 2005. Family Ⅲ, Brucellaceae breed, Murray and smith 1957, 394AL. In:Brenner D J, Krieg N R, Staley J T, Garrity G M eds. 2nd edn. Bergey's Manual of Systematic Bacteriology. Springer, New York.p.370-386.
Gasol J M, del Giorgio P A. 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci.Mar., 64(2):197-224.
Geddes M C. 2005. The ecological health of the North and South Lagoons of the Coorong in July 2004. Report Prepared for the Department of Water, Land and Biodiversity Conservation. SARDI Aquatic Sciences Publication Number RD03/0272-2. South Australian Research and Development Institute (Aquatic Sciences), Adelaide, 29pp.
Ghai R, Pašić L, Fernández A B, Martin-Cuadrado A B, Mizuno C M, McMahon K D, Papke R T, Stepanauskas R, Rodriguez-Brito B, Rohwer F, Sánchez-Porro C, Ventosa A, Rodríguez-Valera F. 2011. New abundant microbial groups in aquatic hypersaline environments. Sci. Rep., 1:135.
Guixa-Boixareu N, Calderón-Paz J I, Heldal M, Bratbak G, Pedrós-Alió C. 1996. Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat.Microb. Ecol., 11(3):215-227.
Han S K, Nedashkovskaya O I, Mikhailov V V, Kim S B, Bae K S. 2003. Salinibacterium amurskyense gen. nov., sp.nov., a novel genus of the family Microbacteriaceae from the marine environment. Int. J. Syst. Evol. Microbiol., 53(6):2 061-2 066.
Henriques I S, Alves A, Tacão M, Almeida A, Cunha Â, Correia A. 2006. Seasonal and spatial variability of free-living bacterial community composition along an estuarine gradient (Ria de Aveiro, Portugal). Estuar. Coast. Shelf Sci., 68(1-2):139-148.
Herlemann D P, Labrenz M, Jürgens K, Bertilsson S, Waniek J J, Andersson A F. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J., 5(10):1 571-1 579.
Hill D, Owens W, Tchounwou P. 2005. Impact of animal waste application on runoff water quality in field experimental plots. Int. J. Environ. Res. Public Health, 2(2):314-321.
Imhoff J F, Süling J. 1996. The phylogenetic relationship among Ectothiorhodospiraceae:a reevaluation of their taxonomy on the basis of 16S rDNA analyses. Arch.Microbiol., 165(2):106-113.
Ivanova E P, Flavier S, Christen R. 2004. Phylogenetic relationships among marine Alteromonas-like Proteobacteria:emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam.nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov.and Psychromonadaceae fam. nov. Int. J. Syst. Evol.Microbiol., 54(5):1 773-1 788.
Jeffries T C, Seymour J R, Gilbert J A, Dinsdale E A, Newton K, Leterme S S C, Roudnew B, Smith R J, Seuront L, Mitchell J G. 2011. Substrate type determines metagenomic profiles from diverse chemical habitats.PLoS One, 6(9):e25173.
Jeffries T C, Seymour J R, Newton K, Smith R J, Seuront L, Mitchell J G. 2012. Increases in the abundance of microbial genes encoding halotolerance and photosynthesis along a sediment salinity gradient.Biogeosciences, 9(2):815-825.
Jolly I D, Williamson D R, Gilfedder M, Walker G R, Morton R, Robinson G, Jones H, Zhang L, Dowling T I, Dyce P, Nathan R J, Nandakumar N, Clarke R, McNeill V. 2001.Historical stream salinity trends and catchment salt balances in the Murray-Darling Basin, Australia. Mar.Freshw. Res., 52(1):53-63.
Jones K, Betaieb M. 1986. The dispersal of nitrogen-fixing enterobacteriaceae from sewage in the waters and sediments of Morecambe Bay, UK. Colloque International de Bacteriologie Marine. IFREMER, É ditions du CNRS, Brest, France. p.525-531.
Kan J J, Suzuki M T, Wang K, Evans S E, Chen F. 2007. High temporal but low spatial heterogeneity of bacterioplankton in the Chesapeake Bay. Appl. Environ. Microbiol., 73(21):6 776-6 789.
Kingsford R T, Walker K F, Lester R E, Young W J, Fairweather P G, Sammut J, Geddes M C. 2011. A Ramsar wetland in crisis-the Coorong, Lower Lakes and Murray Mouth, Australia. Mar. Freshw. Res., 62(3):255-265.
Kiørboe T, Jackson G A. 2001. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria.Limnol. Oceanogr., 46(6):1 309-1 318.
Klatt P, Lamas S. 2000. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem., 267(16):4 928-4 944.
Lamontagne S, McEwan K, Webster I, Ford P, Leaney F, Walker G. 2004. Coorong Lower Lakes and Murray Mouth. Knowledge gaps and knowledge needs for delivering better ecological outcomes. CSIRO Water for a Healthy Country Flagship Report Series. CSIRO, Canberra. 38p.
Lasken R S, Stockwell T B. 2007. Mechanism of chimera formation during the multiple displacement amplification reaction. BMC Biotechnol., 7:19.
Lee S D, Lee D W, Kim J S. 2008. Nocardioides hwasunensis sp. nov. Int. J. Syst. Evol. Microbiol., 58(1):278-281.
Lester R E, Fairweather P G. 2009. Modelling future conditions in the degraded semi-arid estuary of Australia's largest river using ecosystem states. Estuar. Coast. Shelf Sci., 85(1):1-11.
Lozupone C A, Knight R. 2007. Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. USA, 104(27):11 436-11 440.
Magarvey N A, Keller J M, Bernan V, Dworkin M, Sherman D H. 2004. Isolation and characterization of novel marinederived actinomycete taxa rich in bioactive metabolites.Appl. Environ. Microbiol., 70(12):7 520-7 529.
Magurran A E. 2004. Measuring Biological Diversity.Blackwell Science Ltd., Oxford. 264p.
Marie D, Brussaard C P D, Thyrhaug R, Bratbak G, Vaulot D. 1999a. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ.Microbiol., 65(1):45-52.
Marie D, Partensky F, Vaulot D, Brussaard C. 1999b.Numeration of phytoplankton, bacteria, and viruses in marine samples. Curr. Protoc. Cytometry, 10(1):11.11.1-11.11.15.
Meyer F, Paarmann D, D'Souza M, Olson R, Glass E, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards R A. 2008. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinformatics, 9:386.
Mincer T J, Fenical W, Jensen P R. 2005. Culture-dependent and culture-independent diversity within the obligate marine actinomycete genus Salinispora. Appl. Environ.Microbiol., 71(11):7 019-7 028.
Mitchell J G. 2004. Rank-size analysis and vertical phytoplankton distribution patterns. In:Seuront L, Strutton P G eds. Handbook of Scaling Methods in Aquatic Ecology:Measurement, Analysis, Simulation.CRC Press, Boca Raton. p.257-278.
Mudge S, Moss M. 2008. State of the environment report for South Australia 2008. The State of Our Environment:Environmental Protection Authority, Adelaide. 311p.
Newcombe R G. 1998. Improved confidence intervals for the difference between binomial proportions based on paired data. Statist.Med., 17(22):2 635-2 650.
Nieto J J, Fernández-Castillo R, Márquez M C, Ventosa A, Quesada E, Ruiz-Berraquero F. 1989. Survey of metal tolerance in moderately halophilic eubacteria. Appl.Environ. Microbiol., 55(9):2 385-2 390.
Nogales B, Lanfranconi M P, Piña-Villalonga J M, Bosch R. 2011. Anthropogenic perturbations in marine microbial communities. FEMS Microbiol. Rev., 35(2):275-298.
Overbeek R, Begley T, Butler R M, Choudhuri J V, Chuang H Y, Cohoon M, de Crécy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein R E M, Frank E D, Gerdes S, Glass E M, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy A C, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch G D, Rodionov D A, Rückert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y Z, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res., 33(17):5 691-5 702.
Paez J G, Lin M, Beroukhim R, Lee J C, Zhao X J, Richter D J, Gabriel S, Herman P, Sasaki H, Altshuler D, Li C, Meyerson M, Sellers W R. 2004. Genome coverage and sequence fidelity of ϕ29 polymerase-based multiple strand displacement whole genome amplification. Nucleic Acids Res., 32(9):e71.
Parks D H, Beiko R G. 2010. Identifying biologically relevant differences between metagenomic communities.Bioinformatics, 26(6):715-721.
Pǎsić L, Rodriguez-Mueller B, Martin-Cuadrado A B, Mira A, Rohwer F, Rodriguez-Valera F. 2009. Metagenomic islands of hyperhalophiles:the case of Salinibacter ruber.BMC Genomics, 10:570.
Pedrós-Alió C, Calderón-Paz J I, MacLean M H, Medina G, Marrasé C, Gasol J M, Guixa-Boixereu N. 2000. The microbial food web along salinity gradients. FEMS Microbiol. Ecol., 32(2):143-155.
Pernthaler J. 2005. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev.Microbiol., 3(7):537-546.
Persson B C. 1993. Modification of tRNA as a regulatory device. Mol. Microbiol., 8(6):1 011-1 016.
Raux E, Schubert H L, Warren M J. 2000. Biosynthesis of cobalamin (vitamin B12):a bacterial conundrum. Cell.Mol. Life Sci., 57(13-14):1 880-1 893.
Reen F J, Almagro-Moreno S, Ussery D, Boyd E F. 2006. The genomic code:inferring Vibrionaceae niche specialization.Nat. Rev. Microbiol., 4(9):697-704.
Roberts M F. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst., 1:5.
Rodriguez-Brito B, Li L L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, 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, Thurber R V, Willner D, Youle M, Rohwer F. 2010. Viral and microbial community dynamics in four aquatic environments. ISME J., 4(6):739-751.
Ruiz A, Franco J, Villate F. 1998. Microzooplankton grazing in the Estuary of Mundaka, Spain, and its impact on phytoplankton distribution along the salinity gradient.Aquat. Microb. Ecol., 14(3):281-288.
Rusch D B, Halpern A L, Sutton G, Heidelberg K B, Williamson S, Yooseph S, Wu D Y, Eisen J A, Hoffman J M, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter J E, Li K, Kravitz S, Heidelberg J F, Utterback T, Rogers Y H, Falcón L I, Souza V, Bonilla-Rosso G, Eguiarte L E, Karl D M, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari M R, Strausberg R L, Nealson K, Friedman R, Frazier M, Venter J C. 2007.The sorcerer Ⅱ global ocean sampling expedition:northwest Atlantic through eastern Tropical Pacific. PLoS Biol., 5(3):e77.
Sarikhan S, Azarbaijani R, Yeganeh L P, Fazeli A S, Amoozegar M A, Salekdeh G H. 2011. Draft genome sequence of Nesterenkonia sp. strain F, isolated from Aran-Bidgol Salt Lake in Iran. J. Bacteriol., 193(19):5 580.
Schapira M, Buscot M J, Leterme S C, Pollet T, Chapperon C, Seuront L. 2009. Distribution of heterotrophic bacteria and virus-like particles along a salinity gradient in a hypersaline coastal lagoon. Aquat. Microb. Ecol., 54(2):171-183.
Seymour J R, Doblin M A, Jeffries T C, Brown M V, Newton K, Ralph P J, Baird M, Mitchell J G. 2012. Contrasting microbial assemblages in adjacent watermasses associated with the East Australian Current. Environ. Microbiol.Rep., 4(5):548-555.
Seymour J R, Humphreys W F, Mitchell J G. 2007. Stratification of the microbial community inhabiting an anchialine sinkhole. Aquat. Microb. Ecol., 50(1):11-24.
Smith R J, Jeffries T C, Roudnew B, Fitch A J, Seymour J R, Delpin M W, Newton K, Brown M H, Mitchell J G. 2012.Metagenomic comparison of microbial communities inhabiting confined and unconfined aquifer ecosystems.Environ. Microbiol., 14(1):240-253.
Stach E M, Bull A T. 2005. Estimating and comparing the diversity of marine actinobacteria. Antonie van Leeuwenhoek, 87(1):3-9.
Starr T J, Jones M E, Martinez D. 1957. The production of vitamin B12-active substances by marine bacteria. Limnol.Oceanogr., 2(2):114-119.
Stevens H, Brinkhoff T, Rink B, Vollmers J, Simon M. 2007.Diversity and abundance of Gram positive bacteria in a tidal flat ecosystem. Environ. Microbiol., 9(7):1 810-1 822.
Strom S L. 2008. Microbial ecology of ocean biogeochemistry:a community perspective. Science, 320(5879):1 043-1 045.
Tamames J, Abellán J, Pignatelli M, Camacho A, Moya A. 2010. Environmental distribution of prokaryotic taxa.BMC Microbiol., 10:85.
Thurber R V, Haynes M, Breitbart M, Wegley L, Rohwer F. 2009. Laboratory procedures to generate viral metagenomes. Nat. Protocols, 4(4):470-483.
Tourova T P, Spiridonova E M, Berg I A, Slobodova N V, Boulygina E S, Sorokin D Y. 2007. Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences.Int. J. Syst. Evol. Microbiol., 57(10):2 387-2 398.
Webster I T. 2005. An Overview of the Hydrodynamics of the Coorong and Murray Mouth. Technical Report No.#/2005.CSIRO:Water for a Healthy Country National Research Flagship. 33p.
Wu Q L, Zwart G, Schauer M, Kamst-van Agterveld M P, Hahn M W. 2006. Bacterioplankton community composition along a salinity gradient of sixteen highmountain lakes located on the Tibetan Plateau, China.Appl. Environ. Microbiol., 72(8):5 478-5 485.
Yilmaz S, Allgaier M, Hugenholtz P. 2010. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat. Methods, 7(12):943-944.
Yokokawa T, Nagata T, Cottrell M T, Kirchman D L. 2004.Growth rate of the major phylogenetic bacterial groups in the Delaware estuary. Limnol. Oceanogr., 49(5):1 620-1 629.
Zar J H. 1996. Biostatistical Analysis. Prentice-Hall Inc., Upper Saddle River. 944p.