Title: Geochemical constraints on bacteriophage infectivity in terrestrial environments

Journal Article · · ISME Communications

Abstract Lytic phages can be potent and selective inhibitors of microbial growth and can have profound impacts on microbiome composition and function. However, there is uncertainty about the biogeochemical conditions under which phage predation modulates microbial ecosystem function, particularly in terrestrial systems. Ionic strength is critical for infection of bacteria by many phages, but quantitative data is limited on the ion thresholds for phage infection that can be compared with environmental ion concentrations. Similarly, while carbon composition varies in the environment, we do not know how this variability influences the impact of phage predation on microbiome function. Here, we measured the half-maximal effective concentrations (EC50) of 80 different inorganic ions for the infection of E. coli with two canonical dsDNA and ssRNA phages, T4 and MS2, respectively. Many alkaline earth metals and alkali metals enabled lytic infection but the ionic strength thresholds varied for different ions between phages. Additionally, using a freshwater nitrate-reducing microbiome, we found that the ability of lytic phages to influence nitrate reduction end-products depended upon the carbon source as well as ionic strength. For all phage:host pairs, the ion EC50s for phage infection exceeded the ion concentrations found in many terrestrial freshwater systems. Thus, our findings support a model where phages most influence terrestrial microbial functional ecology in hot spots and hot moments such as metazoan guts, drought influenced soils, or biofilms where ion concentration is locally or transiently elevated and nutrients are available to support the growth of specific phage hosts.

Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1995856
Journal Information:
ISME Communications, Journal Name: ISME Communications Journal Issue: 1 Vol. 3; ISSN 2730-6151
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (62)

Soil Phage Ecology: Abundance, Distribution, and Interactions with Bacterial Hosts book September 2010
Caesium accumulation by microorganisms: uptake mechanisms, cation competition, compartmentalization and toxicity journal February 1995
Virus particle adsorption I. Theory of adsorption and experiments on the attachment of particles to non-biological surfaces journal January 1959
The initial steps in infection with coliphage M13 journal November 1964
Stages in phage R17 infection journal March 1970
Bacteria–Phage Interactions in Natural Environments book August 2014
Viruses Inhibit CO 2 Fixation in the Most Abundant Phototrophs on Earth journal June 2016
Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods journal August 2012
Deposition kinetics of bacteriophage MS2 to natural organic matter: Role of divalent cations journal October 2009
Influence of Internal DNA Pressure on Stability and Infectivity of Phage λ journal October 2015
Phage adsorption to bacteria in the light of the electrostatics: A case study using E. coli, T2 and flow cytometry journal May 2013
A relationship between phages and organic carbon in wastewater treatment plant effluents journal August 2022
Role of Cations in Phage Adsorption to Sensitive Bacteria journal July 1957
High abundance of viruses found in aquatic environments journal August 1989
Drought and host selection influence bacterial community dynamics in the grass root microbiome journal July 2017
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life journal August 2018
Re-examination of the relationship between marine virus and microbial cell abundances journal January 2016
The selective pressures on the microbial community in a metal-contaminated aquifer journal December 2018
Selective carbon sources influence the end products of microbial nitrate respiration journal May 2020
Prolonged drought imparts lasting compositional changes to the rice root microbiome journal July 2021
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly journal March 2018
Phage puppet masters of the marine microbial realm journal June 2018
Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing journal December 2018
Mutant phenotypes for thousands of bacterial genes of unknown function journal May 2018
Widespread diminishing anthropogenic effects on calcium in freshwaters journal July 2019
Intracellular ion concentrations and cation-dependent remodelling of bacterial MreB assemblies journal July 2020
Moisture modulates soil reservoirs of active DNA and RNA viruses journal August 2021
Experimental evidence for the impact of soil viruses on carbon cycling during surface plant litter decomposition journal March 2022
Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages journal January 2005
Solid-to-fluid-like DNA transition in viruses facilitates infection journal September 2014
Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands journal November 2022
Bacteriophage T4 whiskers: a rudimentary environment-sensing device. journal September 1975
The First two Steps of the Invasion of host Cells by Bacterial Viruses. ii journal September 1951
Search and clustering orders of magnitude faster than BLAST journal August 2010
PEAR: a fast and accurate Illumina Paired-End reAd mergeR journal October 2013
BioNumbers—the database of key numbers in molecular and cell biology journal October 2009
Ribosomal Database Project: data and tools for high throughput rRNA analysis journal November 2013
Ionic switch controls the DNA state in phage λ journal June 2015
Isolation and Characterization of Bacteriophages for Caulobacter crescentus journal November 1977
Calcium Sensitive and Other Mutants of Bacteriophage P2 journal July 1969
Effects of Calcium on the Lytic Cycle of Bacillus subtilis Phage 41c journal November 1980
UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing posted_content October 2016
The Stability of Phages as a Function of the Ionic Environment, journal January 1953
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies journal October 2015
Deciphering the virus-to-prokaryote ratio (VPR): insights into virus-host relationships in a variety of ecosystems: Deciphering the virus-to-prokaryote ratio journal April 2016
Evidence that viral abundance across oceans and lakes is driven by different biological factors journal June 2008
Isoelectric points of viruses journal January 2010
Comparison of the mineral content of tap water and bottled waters journal March 2001
Models of haloadaptation in bacterial membranes journal July 1986
Enhanced Trehalose Production Improves Growth of Escherichia coli under Osmotic Stress† journal July 2005
Osmolarity and pH Growth Conditions Regulate fim Gene Transcription and Type 1 Pilus Expression in Uropathogenic Escherichia coli journal March 2002
Osmoregulation of alkaline phosphatase synthesis in Escherichia coli K-12 journal November 1983
Bacteriophages of Rhodopseudomonas spheroides : Isolation and Characterization of a Rhodopseudomonas spheroides Bacteriophage journal June 1974
Properties of Caulobacter Ribonucleic Acid Bacteriophage φCb5 journal December 1970
Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust journal December 2019
Removing Noise From Pyrosequenced Amplicons journal January 2011
High cell density cultivation and recombinant protein production with Escherichia coli in a rocking-motion-type bioreactor journal January 2010
Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability journal April 2017
Impact of phages on soil bacterial communities and nitrogen availability under different assembly scenarios journal April 2020
Microbial metal resistance and metabolism across dynamic landscapes: high-throughput environmental microbiology journal January 2017
Viruses and protists cause similar bacterial mortality in coastal seawater journal November 1995
Phage on tap–a quick and efficient protocol for the preparation of bacteriophage laboratory stocks journal January 2016