Effects of Bacteriophages on the Population Dynamics of Four Strains of Pelagic Marine Bacteria

Viral lysis of specific bacterial populations has been suggested to be an important factor for structuring marine bacterioplankton communities. In the present study, the influence of bacteriophages on the diversity and population dynamics of four marine bacterial phage-host systems was studied experimentally in continuous cultures and theoretically by a mathematical model. By use of whole genome DNA hybridization toward community DNA, we analyzed the dynamics of individual bacterial host populations in response to the addition of their specific phage in continuous cultures of mixed bacterial assemblages. In these experiments, viral lysis had only temporary effects on the dynamics and diversity of the individual bacterial host species. Following the initial lysis of sensitive host cells, growth of phage-resistant clones of the added bacteria resulted in a distribution of bacterial strains in the phage-enriched culture that was similar to that in the control culture without phages after about 50-60 h incubation. Consequently, after a time frame of 5-10 generations after lysis, it was the interspecies competition rather than viral lysis of specific bacterial strains that was the driving force in the regulation of bacterial species composition in these experiments. The clonal diversity, on the other hand, was strongly influenced by viral activity, since the clonal composition of the four species in the phage-enriched culture changed completely from phage-sensitive to phage-resistant clones. The model simulation predicted that viral lysis had a strong impact on the population dynamics, the species composition, and the clonal composition of the bacterial community over longer time scales (weeks). However, according to the model, the overall density of bacteria in the system was not affected by phages, since resistant clones complemented the fluctuations caused by viral lysis. Based on the model analysis, we therefore suggest that viral lysis can have a strong influence on the dynamics of bacterial populations in planktonic marine systems.

[1]  David C. Smith,et al.  Blooms of sequence‐specific culturable bacteria in the sea , 1993 .

[2]  T. Frede,et al.  Theoretical models for the control of bacterial growth rate , abundance , diversity and carbon demand , 2022 .

[3]  M. Middelboe,et al.  Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton , 1996, Applied and environmental microbiology.

[4]  T. Thingstad.  Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems , 2000 .

[5]  J. Fuhrman,et al.  Viruses and protists cause similar bacterial mortality in coastal seawater , 1995 .

[6]  Richard E. Lenski,et al.  Effect of resource enrichment on a chemostat community of bacteria and bacteriophage , 1997 .

[7]  R. Lignell,et al.  THEORETICAL MODELS FOR THE CONTROL OF BACTERIAL GROWTH RATE, ABUNDANCE, DIVERSITY AND CARBON DEMAND , 1997 .

[8]  R. Lenski.  Dynamics of Interactions between Bacteria and Virulent Bacteriophage , 1988 .

[9]  G. Bratbak,et al.  High abundance of viruses found in aquatic environments , 1989, Nature.

[10]  M. Middelboe,et al.  Bacterial Growth Rate and Marine Virus–Host Dynamics , 2000, Microbial Ecology.

[11]  J. Ravel,et al.  Hybridization Analysis of Chesapeake Bay Virioplankton , 1999, Applied and Environmental Microbiology.

[12]  B. Eisenstein,et al.  The polymerase chain reaction. A new method of using molecular genetics for medical diagnosis. , 1990, The New England journal of medicine.

[13]  H. Ackermann,et al.  Bacteriophage taxonomy in 1987. , 1987, Microbiological sciences.

[14]  J. Pinhassi,et al.  Dominant marine bacterioplankton species found among colony-forming bacteria , 1997, Applied and environmental microbiology.

[15]  A. M. Chan,et al.  Fluorescently Labeled Virus Probes Show that Natural Virus Populations Can Control the Structure of Marine Microbial Communities , 1995, Applied and environmental microbiology.

[16]  David L. Kirchman,et al.  Degradation of Adsorbed Protein by Attached Bacteria in Relationship to Surface Hydrophobicity , 1990, Applied and environmental microbiology.

[17]  M. Begon,et al.  Ecology: Individuals, Populations and Communities , 1986 .

[18]  R. Lenski.  EXPERIMENTAL STUDIES OF PLEIOTROPY AND EPISTASIS IN ESCHERICHIA COLI. I. VARIATION IN COMPETITIVE FITNESS AMONG MUTANTS RESISTANT TO VIRUS T4 , 1988, Evolution; international journal of organic evolution.

[19]  M. Weinbauer,et al.  Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the gulf of Mexico , 1996, Applied and environmental microbiology.

[20]  J. Fuhrman.  Marine viruses and their biogeochemical and ecological effects , 1999, Nature.

[21]  John B. Waterbury,et al.  Resistance to Co-Occurring Phages Enables Marine Synechococcus Communities To Coexist with Cyanophages Abundant in Seawater , 1993, Applied and environmental microbiology.

[22]  [The polymerase chain reaction (PCR) test]. , 1995, SIDAhora : un proyecto del Departamento de Publicaciones del PWA Coalition, NY.

[23]  J. Ravel,et al.  Population Dynamics of Chesapeake Bay Virioplankton: Total-Community Analysis by Pulsed-Field Gel Electrophoresis , 1999, Applied and Environmental Microbiology.

[24]  R. Lenski,et al.  Constraints on the Coevolution of Bacteria and Virulent Phage: A Model, Some Experiments, and Predictions for Natural Communities , 1985, The American Naturalist.

[25]  M. Begon,et al.  Ecology: Individuals, Populations and Communities , 1986 .

[26]  M. Delbrück,et al.  Mutations of Bacteria from Virus Sensitivity to Virus Resistance. , 1943, Genetics.