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Table 1 Examples of studies that reported/predicted phage-mediated alteration of metabolic function in prokaryotic hosts

From: Host-hijacking and planktonic piracy: how phages command the microbial high seas

Host/s Phage/s; cycle (if known) Modification/Phenomena (molecular; physiological; phenotypic) Observed effect (O) or Predicted effect (P) on host metabolism/ host survival References
Vibrio cholera VPIΦ and CTXΦ; Lysogenic Insertion of VPIΦ results in toxin-coregulated pilus (TCP) expression; TCP-facilitated CTXIΦ insertion into host genome (O) Expression of cholera toxin [67, 68]
Escherichia coli 933 W; Lysogenic to lytic switch Induction of 933 W prophages that encode for both shiga toxin (Stx) and a cleavable repressor (O) Greatly increases stx gene expression, and therefore bacterial production and release of Stx. [65]
Staphylococcus aureus Φ13; Lysogenic Integration of Φ13 genome with beta-toxin gene (hlb) (O) Loss of beta-toxin expression (Note: beta-toxin is a sphingomyelinase) [71]
Escherichia coli λ; Lysogenic λ cI protein expression; cI binds to pckA regulatory region preventing transcription (O) Suppression of phosphoenolpyruvate carboxykinase production & gluconeogenesis; reduced growth rate; predation avoidance [66]
Vibrio harveyi 645; 20; 45 VHML; Lysogenic Integration of VHML genome via transposition (O) Broad suppression of substrate utilization; changes in d-gluconate utilization (625); c-glutamyl transpeptidase activity (20); and sulfatase activity (45) [69, 70]
Listonella pelagia ΦHSIC; Pseudolysogenic Chromosomal integration of prophage (O) Reduction in substrate utilization [21, 110]
Cellulophaga baltica MM#3 ΦSM and ΦST; Lytic On evolution of phage resistance: possible adaptation of amino acid transporters (likely phage receptors) in cell membrane (O) Reduction in ability to metabolise various carbon sources, including many amino acids [111]
Synechococcus WH8109 Cyanophage Syn9; lytic Phage encoded carbon metabolism genes cp12, talC, psbA, zwf, gnd, and nrdA/nrdB, co-expressed in early infection; two-fold increase in NADPH/NADP ratio (P) ‘light reactions’ decoupled from ‘dark reactions; ATP & NADPH directed away from the Calvin Cycle. likely towards phage dNTP biosynthesis [10]
Synechococcus WH8017 S-SM2; lytic Phage encodes genes for photosynthesis (PSII): psbA; psbD, and carbon metabolism genes: gnd; tal; zwf; CP12 (P) Photosynthesis augmented during infection; carbon redirected from glucose and amino acid production to ribose-5P and NAPDH generation (for dNTP synthesis), via PPP-mediated glucose reduction [42, 53]
Cyanobacteria: various Prochlorococcus and Synechococcus strains Various: 42 cultured cyanophages 88% of cyanophage genomes include psbA; 50% code for both psbA and psbD (PSII genes) (P) Boost to phototrophic metabolism during infection. [33]
Cyanobacteria Un-cultured cyanophages Phage-encoded photosystem I genes psaA, B, C, D, E, K and JF (from environmental samples) (P) Channelling of reducing power from respiratory chain towards PSI, possibly for ATP generation [34]
Prochlorococcus MIT9515 P-TIM68; lytic Phage encoded photosystem I and II proteins incorporated into host membrane (O) Photosynthetic capacity maintained; enhanced cyclic electron flow around PSI; (P) Generation additional ATP for phage replication [37]
Vibrios (including V. parahaemolyticus KVP40; lytic Phage ORFs code for: PhoH; putative pyridine nucleotide (NAD+) salvage pathway, and hydrolysis of NADH (P) Facilitates cross-membrane transport of NAD+ precursors, NAD+ synthesis, and cycling of NADH back to precursors. [112]
Various (marine metagenomic Assemblages) Various (marine viral metagenomes) Most abundant putative viral-encoded enzymes: riboreductases; carboxylyases and transferases; psbA genes. (P) Aids scavenging of host nucleotides (e.g. Riboreductases); supports host metabolism during the infection cycle (e.g., carboxylyases; transferases and D1 protein) [113]
Various: from 22 ‘ultra-clean’ viromes in POV dataset Various; classified via protein cluster (PC) generation 35 carbon pathway AMGs, representing a near-full central carbon metabolism gene complement. (P) In oligotrophic environments, AMGs may redirect host carbon flux into energy production and the replication of viral DNA. [53]
Various: from 32 viromes in POV dataset Various; classified via PC generation 32 new viral AMGs (9 core; 20 photic; 3 aphotic): 9 encode Fe-S cluster proteins and genes associated with DNA replication initiation (DnaA), DNA repair (dut; radA) and motility augmentation (psel). (P) Fe-S cluster modulation may drive phage production (in the photic zone); Genes associated with DNA replication and repair, and motility augmentation could assist high-pressure deep-sea survival. [30]
Various: 127 SAGs from uncultivated SUP05 bacteria Various: 69 viral contigs (from SUP05 SAGs) 4 putative AMGs (encoded by 12 viral contigs): phoH (on a bona fide viral contig); 2OG; 2OG-FeII oxygenase, tctA (protein domain only); and dsrC. (P) dsrC likely functional in SUP05 sulfur cycling; characterisation of viral DsrC needed to elucidate roles of viruses in modulating electron transfer during viral infection. [16]
Various: Actinobacteria, proteobacteria (α; δ; γ) Bacteroidetes, Cyanobacteria, Deferribacteres Various, inc. members of T4 (superfamily) and T7 (genus) 243 putative AMGs (95 previously known [6]) including dsrC (11 genes), soxYZ (4 genes), both originating from T4 superfamily; P-II (encodes a nitrogen metabolism regulator) and amoC (encodes ammonia monooxygenase sub-unit) (P) Viral roles in: Sulfur oxidation, via Dsr and Sox pathways; Nitrogen cycling (influenced by P-II), with potential for alternative pathways of N and NH3 uptake during N starvation, and NH3oxidation (via amoC). [47]
Various: 113 genomes (marine bacteria) Various: 64 pro-phage-like elements (21 GTAs) High relative incidence of transcriptional regulatory and repressor-like proteins in putative prophages (comparison: lytic phages) (P) Suppresses non-essential host metabolic activities in unfavourable environments/periods [21]
Listeria monocytogenes ‘A118-like prophage’ (reversible excision) comK gene, encoding L. monocytogenes competence system master regulator, is activated by the excision of A118-like prophage (O) A118-like prophage is excised only when a L. monocytogenes cell is engulfed by a phagosome: the host’s activated competence system facilitates escape, after which prophage reintegrate with host comK gene, deactivating host’s competence system [74]
Anabaena spp.; Nostoc spp. Non-infective ‘prophages’ (x 3; non-reversible excision) Recombinases (prophage-encoded) act to excise prophages from 3 host genes that are involved in nitrogen fixation (nifD; fdxN; hupL) (O) In low nitrogen environments, excision of prophages from host N-fixation genes enables conversion of host cell to form nitrogen-fixing heterocysts [74]
Synechococcus elongatus Cyanophage AS-1 Prevents normal ppGpp accumulation under nutrient limitation, and the corresponding expression of genes for starvation survival (O) Inhibits the host’s natural starvation response under nutrient limitation; (P) promotes metabolic activity otherwise undertaken only when food is plentiful, facilitating phage production in low nutrient conditions [14, 114]
  1. Abbreviations not used in the main text: ORF Open Reading Frame, dut Deoxyuridine triphophatase, radA DNA recombination protein, pseI Pseudaminic synthase, 2OG 2-oxoglutarate; 2OG-FeII oxygenase Fe (II)-dependent oxygenase superfamily, tctA Tripartite tricarboxylate transporter, GTA Gene Transfer Agents