Abstract
Bioassays experiments were conducted to determine the metabolic and community composition response of bacteria to transplants between relatively pristine coastal seawater and sewage-impacted seawater. There were four treatments: (1) pristine seawater bacteria + pristine seawater (Pb + Pw), (2) sewage-impacted bacteria + sewage-impacted water (Sb + Sw), (3) pristine seawater bacteria + sewage-impacted water (Pb + Sw), and (4) sewage-impacted bacteria + pristine seawater (Sb + Pw). Sewage-derived DOC was more labile and readily utilized by bacteria, which favored the growth of high nucleic acid (HNA) bacteria, resulting in high bacterial production (BP, 113 ± 4.92 to 130 ± 15.8 μg C l−1 day−1) and low respiration rate (BR, <67 ± 11.3 μg C l−1 day−1), as well as high bacterial growth efficiency (BGE, 0.68 ± 0.09 to 0.71 ± 0.05). In contrast, at the relatively pristine site, bacteria utilized natural marine-derived dissolved organic matter (DOM) at the expense of lowering their growth efficiency (BGE, <0.32 ± 0.02) with low BP (<62 ± 6.3 μg C l−1 day−1) and high BR 133 ± 14.2 μg C l−1 day−1). Sewage DOM input appeared to alter the partitioning of carbon between respiration and production of bacteria, resulting in a shift toward higher BGE, which would not enhance oxygen consumption. Taxonomic classification based on 454 pyrosequencing reads of the 16S rRNA gene amplicons revealed that changes in bacterial community structure occurred when seawater bacteria were transferred to the eutrophic sewage-impacted water. Sewage DOM fueled the growth of Gammma-proteobacteria and Epsilson-proteobacteria and reduced the bacterial richness, but the changes in the community were not apparent when sewage-impacted bacteria were transferred to pristine seawater.
Similar content being viewed by others
References
Alonso-Sáez L, Unanue M, Latatu A, Azua I, Ayo B, Artolozaga I, Iriberri J (2009) Changes in marine prokaryotic community induced by varying types of dissolved organic matter and subsequent grazing pressure. J Plankton Res 31(11):1373–1383
Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nature Rev Microb 5:782–791
Benner R, Pakulski JD, McCarthy M, Hedges JI, Hatcher PG (1992) Bulk chemical characteristics of dissolved organic matter in the ocean. Science 255(5051):1561–1564
Bonilla-Findji O, Rochelle-Newall E, Weinbauer MG, Pizay MD, Kerros ME, Gattuso JP (2009) Effects of seawater–freshwater cross-transplantation on viral dynamics and bacterial diversity and production. Aquat Microb Ecol 54:1–11
Broom M, Chiu G, Lee A (2003) Long-term water quality trends in Hong Kong. In: Morton B (ed) Perspectives on marine environment change in Hong Kong and southern China, 1977–2001. Hong Kong University Press, Hong Kong, pp 534
Carlson CA, del Giorgio PA, Herndl GJ (2007) Microbes and the dissipation of energy and respiration: from cells to ecosystems. Oceanography 20:89–100
Carlson CA, Ducklow HW (1996) Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat Microb Ecol 10:69–85
Church MJ (2008) Resource control of bacterial dynamics in the sea. In Kirchman DL (ed) Microbial ecology of the ocean. Wiley-Liss Inc., New York, pp 335–382.
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucl Acids Res 37(Database issue):D141–D145
Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga–Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microb 66(4):1692–1697
del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Evol S 29:503–541
del Giorgio PA, Cole JJ (2000) Bacterial energetics and growth efficiency. In: Kirchman KL (ed) Microbial ecology of the ocean. Wiley-Liss Inc., New York, pp 289–325.
del Giorgio PA, Condon R, Bouvier T, Longnecker K, Bouvier C, Sherr E, Gasol JM (2011) Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a northeastern Pacific inshore–offshore transect. Limnol Oceanogr 56(1):1–16
Findlay SED, Sinsabaugh RL, Soczak WV, Hoostal M (2003) Metabolic and structural response of hyporheic microbial communities to variations in supply of dissolved organic matter. Limnol Oceanogr 48(4):1608–1617
Gasol JM, Alonso-Sáez JPL, Ducklow H, Herndl GJ, Koblížek M, Labrenz M, Luo Y, Morán XAG, Reinthaler T, Simon M (2008) Towards a better understanding of microbial carbon flux in the sea. Aquat Microb Ecol 53:21–38
Grasshoff KM, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Weinheim, Verlag Chemie
Gray NF (2004) Biology of wastewater treatment, 2nd ed. Series on environmental science and management, Vol. 4. Imperial College Press, London, p 1395
He BY, Dai MH, Zhai WD, Wang LF, Wang KJ, Chen JH, Lin JR, Han AQ, Cu YP (2010) Distribution, degradation and dynamics of dissolved organic carbon and its major compound classes in the Pearl River estuary, China. Mar Chem 119:52–64
Holmquist L, Kjelleberg S (1993) Changes in viability, respiratory activity and morphology of the marine Vibrio sp. Strain S14 during starvation of individual nutrients and subsequent recovery. FEMS Microbiol Ecol 12(4):215–223
Hopkinson CS Jr (1985) Shallow-water benthic and pelagic metabolism: evidence of heterotrophy in the nearshore Georgia Bight. Mar Biol 87:19–32
Kirchman DL, Ditter AI, Findley SEG, Fischer D (2004) Changes in bacterial activity and community structure in response to dissolved organic matter in the Hudson River, New York. Aquat Microb Ecol 35:243–257
Kirchman DL, Rich JH (1997) Regulation of bacterial growth rates of dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb Ecol 33(1):11–20
Knap A, Michaels A, Close A, Ducklow H, Dickson A (1996) (eds) Protocols for the Joint Global Ocean Flux Study (JGOFS) core measurements. JGOFS report No 19. Reprint of the IOC Manual and Guides NO 29 (1994). UNESCO, Paris.
Langenheder S, Kisand V, Lindström ES, Wikner J, Tranvik LJ (2004) Growth dynamics within bacterial communities in riverine and estuarine batch cultures. Aquat Microb Ecol 37:137–148
Lebaron P, Servais P, Agogué H, Courties C, Joux F (2001) Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol 67:1775–1782
Marie D, Partensky F, Jacquet S, 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. Appl Environ Microb 63(1):186–193
Marie D, Brussaard CPD, Thyrhaug R, Bratbak G, Vaulot D (1999) Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 65:45–52
Middelboe M, Borch NH, Kirchman DL (1995) Bacterial utilization of dissolved free amino acids dissolved combined amino acids and ammonium in the Delaware Bay estuary: effects of carbon and nitrogen limitation. Mar Ecol Prog Ser 128:109–120
Morán XA, Ducklow HW, Erickson M (2011) Single-cell physiological structure and growth rates of heterotrophic bacteria in a temperate estuary (Waquoit Bay, Massachusetts). Limnol Oceanogr 56:37–48
Motegi C, Nagata T, Miki T, Weinbauer MG, Legendre L, Rassoulzadegan F (2009) Viral control of bacterial growth efficiency in marine pelagic environments. Limnol Oceanogr 54(6):1901–1910
Outdot CR, Gerard R, Morin P, Gningue I (1988) Precise shipboard determination of dissolved oxygen (Winkler procedure) for productivity studies with a commercial system. Limnol Oceanogr 33(1):146–150
Pedrós-Alió C, Calderón-Paz J, Guixa-Boixereu N, Estrada M, Gasol JM (1999) Bacterioplankton and phytoplankton biomass and production during summer stratification in the northwestern Mediterranean Sea. Deep Sea Res I 46(6):985–1019
Pinhassi J, Berman T (2003) Differential growth response of colony-forming α and γ-proteobacteria in dilution culture and nutrient addition experiments from Lake Kinneret (Israel), the Eastern Mediterranean Sea, and the Gulf of Eilat. Appl Environ Microb 69(1):199–211
Reinthaler T, Winter C, Herndl GJ (2005) Relationship between bacterioplankton richness, respiration and production in the southern North Sea. Appl Environ Microb 71(5):2260–2266
Rodriguez-Brito B, Li LL, 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 AB, Mira A, Nulton J, Pašić L, Rayhawk S, Rodriguez-Mueller J, Rodriguez-Valera F, Salamon P, Srinagesh S, Thingstad TF, Tran T, Thurber RV, Willner D, Youle M, Rohwer F (2010) Viral and microbial community dynamics in four aquatic environments. The ISME J 4:739–751
Russell JB, Cook GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59(1):48–62
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541
Strickland JDH, Parsons TR (1968) Determination of reactive nitrate. In: A practical handbook of seawater analysis. Bull Fish Res Board Can 167:71–75
Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27
Winter C, Smit A, Herndl GJ, Weinbauer MG (2005) Linking bacterial richness with viral abundance and prokaryotic activity. Limnol Oceanogr 50:968–977
Wu M, Song L, Ren J, Kan J, Qian PY (2004) Assessment of microbial dynamics in the Pearl River estuary by 16S rRNA terminal restriction fragment analysis. Cont Shelf Res 24:1925–1934
Xu J, Yin K, Ho AYT, Lee JHW, Anderson DM, Harrison PJ (2009) Nutrient limitation in Hong Kong waters inferred from comparison of nutrient ratios, bioassays and 33P turnover times. Mar Ecol Prog Ser 388:81–97
Zhang R, Weinbauer MG, Qian PY (2007) Viruses and flagellates sustain apparent richness and reduce biomass accumulation of bacterioplankton in coastal marine waters. Environ Microbiol 9:3008–3018
Acknowledgements
Financial support for this research was provided by the University Grants Committee of Hong Kong AoE project (AoE/P-04/04-4-II) and Research Grants Council of Hong Kong’s General Research Fund (661911 and 661610). We thank Ms. Candy Lee for helping to count viruses with a flow cytometer.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Xu, J., Jing, H., Kong, L. et al. Effect of Seawater–Sewage Cross-Transplants on Bacterial Metabolism and Diversity. Microb Ecol 66, 60–72 (2013). https://doi.org/10.1007/s00248-013-0207-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-013-0207-2