Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a “giant virus”

English version

Autoři: Eric R. Gann ^aff001; P. Jackson Gainer ^aff002; Todd B. Reynolds ^aff001; Steven W. Wilhelm ^aff001
Působiště autorů: Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America ^aff001; Department of Biology, Tennessee Wesleyan University, Athens, Tennessee, United States of America ^aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226758

Souhrn

The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980’s, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m^-2 s^-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m^-2 s^-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. Overall, these studies provide a framework for understanding light effects on infection dynamics over the course of the summer months when A. anophagefferens blooms occur.

Klíčová slova:

Algae – Biosynthesis – Light – Photons – Ribosomes – Transcriptome analysis – Epifluorescence microscopy – RNA helicases

Zdroje

1. Sieburth JM, Johnson PW, Hargraves PE. Ultrastructure and ecology of Aureococcus anophagefferens gen. et. sp. nov. (Chrysophyceae)—the dominant picoplankter during a bloom in Narragansett Bay, Rhode-Island, Summer 1985. J. Phycol. 1988; 24(3):416–25. doi: 10.1111/j.1529-8817.1988.tb04485.x WOS:A1988Q093500018.

2. Gastrich MD, Anderson OR, Cosper EM. Viral-like particles (VLPS) in the alga, Aureococcus anophagefferens (Pelagophyceae), during 1999–2000 brown tide blooms in Little Egg Harbor, New Jersey. Estuaries. 2002; 25(5):938–43. doi: 10.1007/Bf02691342 WOS:000178996800005.

3. Gobler CJ, Berry DL, Dyhrman ST, Wilhelm SW, Salamov A, Lobanov AV, et al. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. P Natl Acad Sci. 2011; 108(11): 4352–7. doi: 10.1073/pnas.1016106108 21368207; PubMed Central PMCID: PMC3060233.

4. Gobler CJ, Sunda WG. Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae. 2012; 14: 36–45. doi: 10.1016/j.hal.2011.10.013 WOS:000300818000004.

5. Popels LC, Cary SC, Hutchins DA, Forbes R, Pustizzi F, Gobler CJ, et al. The use of quantitative polymerase chain reaction for the detection and enumeration of the harmful alga Aureococcus anophagefferens in environmental samples along the United States East Coast. Limnol Oceanogr-Meth. 2003; 1: 92–102. doi: 10.4319/lom.2003.1.92 WOS:000202872600011.

6. Zhang QC, Qiu LM, Yu RC, Kong FZ, Wang YF, Yan T, et al. Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae. 2012; 19: 117–24. doi: 10.1016/j.hal.2012.06.007 WOS:000309033700015.

7. Probyn T, Pitcher G, Pienaar R, Nuzzi R. Brown tides and mariculture in Saldanha Bay, South Africa. Mar Pollut Bull. 2001; 42(5): 405–8. doi: 10.1016/s0025-326x(00)00170-3 WOS:000169401400020. 11436821

8. Popels LC, Hutchins DA. Factors affecting dark survival of the brown tide alga Aureococcus anophagefferens (Pelagophyceae). J. Phycol. 2002; 38(4): 738–44. doi: 10.1046/j.1529-8817.2002.01115.x WOS:000177836500014.

9. Gastrich MD, Leigh-Bell JA, Gobler CJ, Anderson OR, Wilhelm SW, Bryan M. Viruses as potential regulators of regional brown tide blooms caused by the alga, Aureococcus anophagefferens. Estuaries. 2004; 27(1): 112–9. doi: 10.1007/Bf02803565 WOS:000221048900010.

10. Rowe JM, Dunlap JR, Gobler CJ, Anderson OR, Gastrich MD, Wilhelm SW. Isolation of a non-phage-like lytic virus infecting Aureococcus anophagefferens. J. Phycol. 2008; 44(1): 71–6. doi: 10.1111/j.1529-8817.2007.00453.x 27041042.

11. Moniruzzaman M, Gann ER, Wilhelm SW. Infection by a giant virus (AaV) induces widespread physiological reprogramming in Aureococcus anophagefferens CCMP1984—A Harmful Bloom Algae. Front Microbiol. 2018; 9: 752. doi: 10.3389/fmicb.2018.00752 29725322; PubMed Central PMCID: PMC5917014.

12. Moniruzzaman M, LeCleir GR, Brown CM, Gobler CJ, Bidle KD, Wilson WH, et al. Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host-virus coevolution. J. Virol. 2014; 466–467: 60–70. doi: 10.1016/j.virol.2014.06.031 25035289.

13. Moniruzzaman M, Gann ER, LeCleir GR, Kang Y, Gobler CJ, Wilhelm SW. Diversity and dynamics of algal Megaviridae members during a harmful brown tide caused by the pelagophyte, Aureococcus anophagefferens. FEMS Microbiol Ecol. 2016; 92(5): fiw058 doi: 10.1093/femsec/fiw058 WOS:000377473000010. 26985013

14. Moniruzzaman M, Wurch LL, Alexander H, Dyhrman ST, Gobler CJ, Wilhelm SW. Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics. Nat Commun. 2017; 8: 16054 doi: 10.1038/ncomms16054 WOS:000404227600001. 28656958

15. Vardi A, Haramaty L, Van Mooy BAS, Fredricks HF, Kimmance SA, Larsen A, et al. Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. P Natl Acad Sci USA. 2012; 109(47): 19327–32. doi: 10.1073/pnas.1208895109 WOS:000311997200064. 23134731

16. Wilhelm SW, Weinbauer MG, Suttle CA, Jeffrey WH. The role of sunlight in the removal and repair of viruses in the sea. Limnol Oceanogr. 1998; 43(4): 586–92. doi: 10.4319/lo.1998.43.4.0586 WOS:000075320300004.

17. Long AM, Short SM. Seasonal determinations of algal virus decay rates reveal overwintering in a temperate freshwater pond. ISME J. 2016; 10(7): 1602–12. doi: 10.1038/ismej.2015.240 26943625; PubMed Central PMCID: PMC4918447.

18. Baudoux AC, Brussaard CPD. Influence of irradiance on virus-algal host interactions. J. Phycol. 2008; 44(4): 902–8. doi: 10.1111/j.1529-8817.2008.00543.x WOS:000258099000008. 27041608

19. Van Etten JL, Burbank DE, Xia Y, Meints RH. Growth-Cycle of a Virus, Pbcv-1, That Infects Chlorella-Like Algae. J. Virol. 1983; 126(1): 117–25. doi: 10.1016/0042-6822(83)90466-X WOS:A1983QM68100009.

20. Piedade GJ, Wesdorp EM, Montenegro-Borbolla E, Maat DS, Brussaard CPD. Influence of irradiance and temperature on the virus MpoV-45T infecting the Arctic picophytoplankter Micromonas polaris. Viruses. 2018; 10(12); 676. doi: 10.3390/v10120676 WOS:000455313100015. 30501060

21. Clasen JL, Elser JJ. The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella Virus-1. Freshwater Biol. 2007; 52(1): 112–22. doi: 10.1111/j.1365-2427.2006.01677.x WOS:000242660200010.

22. Gobler CJ, Anderson OR, Gastrich MD, Wilhelm SW. Ecological aspects of viral infection and lysis in the harmful brown tide alga Aureococcus anophagefferens. Aquat Microb Ecol. 2007;47(1):25–36. doi: 10.3354/ame047025 WOS:000246081700003.

23. Brown CM, Bidle KD. Attenuation of virus production at high multiplicities of infection in Aureococcus anophagefferens. J. Virol. 2014; 466–467: 71–81. doi: 10.1016/j.virol.2014.07.023 25104555.

24. Milligan AJ, Cosper EM. Growth and photosynthesis of the 'brown tide' microalga Aureococcus anophagefferens in subsaturating constant and fluctuating irradiance. Mar Ecol Prog Ser. 1997; 153: 67–75. doi: 10.3354/meps153067 WOS:A1997XR97400007.

25. Frischkorn KR, Harke MJ, Gobler CJ, Dyhrman ST. De novo assembly of Aureococcus anophagefferens transcriptomes reveals diverse responses to the low nutrient and low light conditions present during blooms. Front Microbiol. 2014; 5: 375. doi: 10.3389/fmicb.2014.00375 25104951; PubMed Central PMCID: PMC4109616.

26. Pustizzi F, MacIntyre H, Warner ME, Hutchins DA. Interaction of nitrogen source and light intensity on the growth and photosynthesis of the brown tide alga Aureococcus anophagefferens. Harmful Algae. 2004; 3(4): 343–60. doi: 10.1016/j.hal.2004.06.006 WOS:000225525500007.

27. Lomas MW, Glibert PM, Berg GM, Burford M. Characterization of nitrogen uptake by natural populations of Aureococcus anophagefferens (Chrysophyceae) as a function of incubation duration, substrate concentration, light, and temperature. J. Phycol. 1996; 32(6): 907–16. doi: 10.1111/j.0022-3646.1996.00907.x WOS:A1996WB44100003.

28. Gann ER. ASP12A Recipe for culturing Aureococcus anophagefferens. 2016. Protocols.io. doi: 10.17504/protocols.io.f3ybqpw

29. Gann E. Plaque assay for the Aureococcus anophagefferens Virus (AaV). Protocols.io. doi: 10.17504/protocols.io.g2nbyde

30. Schroeder DC, Oke J, Malin G, Wilson WH. Coccolithovirus (Phycodnaviridae): Characterisation of a new large dsDNA algal virus that infects Emiliania huxleyi. Arch Virol. 2002; 147(9): 1685–98. doi: 10.1007/s00705-002-0841-3 WOS:000178041200002. 12209309

31. Cottrell MT, Suttle CA. Dynamics of a lytic virus infecting the photosynthetic marine picoflagellate Micromonas-pusilla. Limnol Oceanogr. 1995; 40(4): 730–9. doi: 10.4319/lo.1995.40.4.0730 WOS:A1995RM27700010.

32. Jarvis B, Wilrich C, Wilrich PT. Reconsideration of the derivation of Most Probable Numbers, their standard deviations, confidence bounds and rarity values. J Appl Microbiol. 2010; 109(5): 1660–7. doi: 10.1111/j.1365-2672.2010.04792.x WOS:000282813800017. 20602657

33. Noble RT, Fuhrman JA. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol. 1998; 14(2): 113–8. doi: 10.3354/ame014113 WOS:000072138900001.

34. Wu ZJ, Jenkins BD, Rynearson TA, Dyhrman ST, Saito MA, Mercier M, et al. Empirical bayes analysis of sequencing-based transcriptional profiling without replicates. BMC Bioinformatics. 2010; 11; 564. doi: 10.1186/1471-2105-11-564 WOS:000285186600001. 21080965

35. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26(1): 139–40. doi: 10.1093/bioinformatics/btp616 WOS:000273116100025. 19910308

36. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017; 45(D1): D353–D61. doi: 10.1093/nar/gkw1092 WOS:000396575500052. 27899662

37. Team RC. A language and environment for statistical computing. Vienna, Austria: Computing RFfS; 2014.

38. Bratbak G, Jacobsen A, Heldal M, Nagasaki K, Thingstad F. Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat Microb Ecol. 1998; 16(1): 1–9. doi: 10.3354/ame016001 WOS:000076737700001.

39. Tarutani K, Nagasaki K, Yamaguchi M. Virus adsorption process determines virus susceptibility in Heterosigma akashiwo (Raphidophyceae). Aquat Microb Ecol. 2006; 42(3): 209–13. doi: 10.3354/ame042209 WOS:000237243000001.

40. Maat DS, de Blok R, Brussaard CPD. Combined phosphorus limitation and light stress prevent viral proliferation in the phytoplankton species Phaeocystis globosa, but not in Micromonas pusilla. Front Mar Sci. 2016; 3: 160. doi: 10.3389/fmars.2016.00160 WOS:000457358000157.

41. Hou Y, Zhang H, Miranda L, Lin S. Serious overestimation in quantitative PCR by circular (supercoiled) plasmid standard: microalgal pcna as the model gene. PloS ONE. 2010; 5(3): e9545. doi: 10.1371/journal.pone.0009545 20221433; PubMed Central PMCID: PMC2832698.

42. Popels LC, MacIntyre HL, Warner ME, Zhang YH, Hutchins DA. Physiological responses during dark survival and recovery in Aureococcus anophagefferens (Pelagophyceae). J. Phycol. 2007; 43(1): 32–42. doi: 10.1111/j.1529-8817.2006.00303.x WOS:000244004300004.

43. Thamatrakoln K, Talmy D, Haramaty L, Maniscalco C, Latham JR, Knowles B, et al. Light regulation of coccolithophore host-virus interactions. New Phytol. 2019; 221(3): 1289–302. doi: 10.1111/nph.15459 30368816.

44. Kief DR, Warner JR. Coordinate control of syntheses of ribosomal ribonucleic-scid and ribosomal-proteins during nutritional shift-up in Saccharomyces cerevisiae. Moll Cell Bio. 1981;1(11):1007–15. doi: 10.1128/Mcb.1.11.1007 WOS:A1981MP68100005. 7050661

45. Simonin D, Diaz JJ, Masse T, Madjar JJ. Persistence of ribosomal protein synthesis after infection of HeLa cells by herpes simplex virus type 1. J Gen Virol. 1997; 78: 435–43. doi: 10.1099/0022-1317-78-2-435 WOS:A1997WF42200019. 9018067

46. Puxty RJ, Evans DJ, Millard AD, Scanlan DJ. Energy limitation of cyanophage development: implications for marine carbon cycling. ISME J. 2018; 12(5): 1273–86. doi: 10.1038/s41396-017-0043-3 WOS:000431321500011. 29379179

47. Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature. 2016; 532(7600): 465–70. doi: 10.1038/nature16942 26863193; PubMed Central PMCID: PMC4851848.

48. Lawrence JE, Suttle CA. Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat Microb Ecol. 2004; 37(1): 1–7. doi: 10.3354/ame037001 WOS:000225336500001.

49. Kana TM, Lomas MW, MacIntyre HL, Cornwell JC, Gobler CJ. Stimulation of the brown tide organism, Aureococcus anophagefferens, by selective nutrient additions to in situ mesocosms. Harmful Algae. 2004; 3(4): 377–88. doi: 10.1016/j.hal.2004.06.008 WOS:000225525500009.

50. Maat DS, Brussaard CPD. Both phosphorus- and nitrogen limitation constrain viral proliferation in marine phytoplankton. Aquat Microb Ecol. 2016; 77(2): 87–97. doi: 10.3354/ame01791 WOS:000384308000003.

51. Wurch LL, Haley ST, Orchard ED, Gobler CJ, Dyhrman ST. Nutrient-regulated transcriptional responses in the brown tide-forming alga Aureococcus anophagefferens. Environ Microbiol. 2011; 13(2): 468–81. doi: 10.1111/j.1462-2920.2010.02351.x 20880332; PubMed Central PMCID: PMC3282463.

52. Wurch LL, Alexander H, Frischkorn KR, Haley ST, Gobler CJ, Dyhrman ST. Transcriptional shifts highlight the role of nutrients in harmful brown tide dynamics. Front Microbiol. 2019;10. 136. doi: 10.3389/fmicb.2019.00136 WOS:000458412300001. 30809203

Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a “giant virus”

Souhrn

Klíčová slova:

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