深海病毒的特征及其生态学功能探讨
|
摘要
病毒是自然环境中丰度最高的生物类群,对海洋生态系统中的物质能量循环和种群平衡调节发挥着不可或缺的作用.深海是海洋生态系统的重要组成部分,深海微生物面临多重极端环境压力.近年来,深海病毒相关的研究揭示了其在深海环境中的高丰度和多样性,以及其重要的生态学功能.本文从深海病毒的主要特征、与环境因子的相关性、深海病毒的分离与鉴定及其生理及生态功能这4个方面进行了概述,并对未来研究的潜在方向做了展望.
Believed to be the most abundant(～1030) biological agents in the ocean, viruses play an important role in microbial metabolism, prokaryotic mortality, and nutrient recycling in marine ecosystems, thereby significantly influencing the geochemical cycles of our planet. The importance of viruses in the surface ocean has been well recognized, however we are just beginning to understand the viral role and the underlying mechanism in the deep ocean. As an essential part of the marine environment, the abyssal ocean has extensive material and energy exchanges with the upper ocean and the deep biosphere, and they constitute an integral whole of the marine ecosystem. With an average depth of approximately 3800 m,the benthic environment is characterized by total darkness, low temperature(<4oC), and high hydrostatic pressure(>10 MPa). The deep-sea inhabited microorganisms, including viruses, are believed to develop unique strategy to survive under multiple extreme environmental stresses. Studies on deep-sea viruses have revealed their abundance, diversity, and important ecological functions. In this review, advances in research on deep-sea viruses are summarized into four parts:general features, relationship between environmental factors and deep-sea viruses, isolation and characterization of representative viruses, and significant influences of the viriobenthos on the physiological and ecological function of deepsea microorganisms. In general, the functions of viruses in the deep-sea environment mainly include two aspects: First, the regulation of material and energy cycle(viral shunt) and the dynamic change in ecosystem composition(balance of microbial communities) modulated by viral lysis; second, the expression of viral metabolic related genes(auxiliary metabolism) and the effect of viruses on host physiological activities(environmental adaptability). The former has been widely recognized, but the influence and molecular mechanism of the latter in the extreme deep-sea environment need to be further investigated. Here, we propose research directions and challenges in this field to undertake in future studies.Notably, the relationship between environmental factors and deep-sea viruses remains poorly understood. A deep-sea viralhost model system must be developed to investigate the underlying regulatory mechanism of gene expression and the interaction between deep-sea viruses and their hosts under extreme environmental conditions. At present, the number of isolated deep-sea viruses is less than 30, which is below 1% of the total number of viruses in the International Virus Classification Database. In terms of classification, most of the isolated deep-sea viruses belong to Caudovirales, and nearly no representatives have been identified yet from other viral orders. Furthermore, deep-sea viruses have been rarely subjected to in-depth study possibly because of very few benthic microorganisms with genetic operating system. In addition to maximizing the use of existing virus-host systems, scholars must focus on isolating other representative deepsea viruses. Although our understanding on viriobenthos is still far from complete, data provided here encourage us to hypothesize that viruses are the key component of the benthic ecosystem and play an indispensable role in the deep ocean and deep biosphere.
Believed to be the most abundant(～1030) biological agents in the ocean, viruses play an important role in microbial metabolism, prokaryotic mortality, and nutrient recycling in marine ecosystems, thereby significantly influencing the geochemical cycles of our planet. The importance of viruses in the surface ocean has been well recognized, however we are just beginning to understand the viral role and the underlying mechanism in the deep ocean. As an essential part of the marine environment, the abyssal ocean has extensive material and energy exchanges with the upper ocean and the deep biosphere, and they constitute an integral whole of the marine ecosystem. With an average depth of approximately 3800 m,the benthic environment is characterized by total darkness, low temperature(<4oC), and high hydrostatic pressure(>10 MPa). The deep-sea inhabited microorganisms, including viruses, are believed to develop unique strategy to survive under multiple extreme environmental stresses. Studies on deep-sea viruses have revealed their abundance, diversity, and important ecological functions. In this review, advances in research on deep-sea viruses are summarized into four parts:general features, relationship between environmental factors and deep-sea viruses, isolation and characterization of representative viruses, and significant influences of the viriobenthos on the physiological and ecological function of deepsea microorganisms. In general, the functions of viruses in the deep-sea environment mainly include two aspects: First, the regulation of material and energy cycle(viral shunt) and the dynamic change in ecosystem composition(balance of microbial communities) modulated by viral lysis; second, the expression of viral metabolic related genes(auxiliary metabolism) and the effect of viruses on host physiological activities(environmental adaptability). The former has been widely recognized, but the influence and molecular mechanism of the latter in the extreme deep-sea environment need to be further investigated. Here, we propose research directions and challenges in this field to undertake in future studies.Notably, the relationship between environmental factors and deep-sea viruses remains poorly understood. A deep-sea viralhost model system must be developed to investigate the underlying regulatory mechanism of gene expression and the interaction between deep-sea viruses and their hosts under extreme environmental conditions. At present, the number of isolated deep-sea viruses is less than 30, which is below 1% of the total number of viruses in the International Virus Classification Database. In terms of classification, most of the isolated deep-sea viruses belong to Caudovirales, and nearly no representatives have been identified yet from other viral orders. Furthermore, deep-sea viruses have been rarely subjected to in-depth study possibly because of very few benthic microorganisms with genetic operating system. In addition to maximizing the use of existing virus-host systems, scholars must focus on isolating other representative deepsea viruses. Although our understanding on viriobenthos is still far from complete, data provided here encourage us to hypothesize that viruses are the key component of the benthic ecosystem and play an indispensable role in the deep ocean and deep biosphere.
引文
1 Goyal S M,Gerba C P,Bitton G.Phage Ecology.New York:John Wiley&Sons,1987
2 Bergh O,B?rsheim K Y,Bratbak G,et al.High abundance of viruses found in aquatic environments.Nature,1989,340:467-468
3 Fuhrman J A.Marine viruses and their biogeochemical and ecological effects.Nature,1999,399:541-548
4 Suttle C A.Viruses in the sea.Nature,2005,437:356-361
5 Wilhelm S W,Suttle C A.Viruses and nutrient cycles in the sea.Bio Science,1999,49:781-788
6 Breitbart M,Bonnain C,Malki K,et al.Phage puppet masters of the marine microbial realm.Nat Microbiol,2018,3:754-766
7 Lu L F,Zhang R,Xu J,et al.Influence of virus upon the marine bacterial metabolism and its biogeochemical effects(in Chinese).Adv Ear Sci,2018,33:225-235[卢龙飞,张锐,徐杰,等.病毒对海洋细菌代谢的影响及其生物地球化学效应.地球科学进展,2018,33:225-235]
8 Wang H,Bai S J,Cai W W,et al.Modulating marine ecosystem by marine viruses-A review(in Chinese).Acta Microbiol Sin,2009,49:551-559[王慧,柏仕杰,蔡雯蔚,等.海洋病毒-海洋生态系统结构与功能的重要调控者.微生物学报,2009,49:551-559]
9 Li S K,Li C B.The progress of the effects of ocean virus on microbial community composition and biogeochemical cycles(in Chinese).Mar Sci,2013,37:117-121[李升康,李传标.海洋病毒在海洋微生物群落及生物地球化学循环中的作用研究进展.海洋科学,2013,37:117-121]
10 Zhang Y Y,Huang C X,Yang J,et al.Interactions between marine microorganisms and their phages.Chin Sci Bull,2011,56:1770-1777
11 Gage J D,Tyler P A.Deep-sea Biology:A Natural History of Organisms at the Deep-Sea Floor.Cambridge:Cambridge University Press,1992
12 Whitman W B,Coleman D C,Wiebe W J.Prokaryotes:The unseen majority.Proc Natl Acad Sci USA,1998,95:6578-6583
13 Hara S,Koike I,Terauchi K,et al.Abundance of viruses in deep oceanic waters.Mar Ecol Prog Ser,1996,145:269-277
14 Magagnini M,Corinaldesi C,Monticelli L S,et al.Viral abundance and distribution in mesopelagic and bathypelagic waters of the Mediterranean Sea.Deep Sea Res Part I-Oceanogr Res Pap,2007,54:1209-1220
15 Arístegui J,Gasol J M,Duarte C M,et al.Microbial oceanography of the dark ocean’s pelagic realm.Limnol Oceanogr,2009,54:1501-1529
16 Nunoura T,Takaki Y,Hirai M,et al.Hadal biosphere:Insight into the microbial ecosystem in the deepest ocean on earth.Proc Natl Acad Sci USA,2015,112:E1230-E1236
17 Danovaro R,Serresi M.Viral density and virus-to-bacterium ratio in deep-sea sediments of the Eastern Mediterranean.Appl Environ Micro Biol,2000,66:1857-1861
18 Danovaro R,Dell’Anno A,Corinaldesi C,et al.Major viral impact on the functioning of benthic deep-sea ecosystems.Nature,2008,454:1084-1087
19 Yoshida M,Takaki Y,Eitoku M,et al.Metagenomic analysis of viral communities in(hado)pelagic sediments.PLo S One,2013,8:e57271
20 Ortmann A C,Suttle C A.High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality.Deep Sea Res Part I-Oceanogr Res Pap,2005,52:1515-1527
21 Ray J,Dondrup M,Modha S,et al.Finding a needle in the virus metagenome haystack-Micro-metagenome analysis captures a snapshot of the diversity of a bacteriophage armoire.PLo S One,2012,7:e34238
22 Kellogg C A.Enumeration of viruses and prokaryotes in deep-sea sediments and cold seeps of the Gulf of Mexico.Deep Sea Res Part II-Topical Stud Oceanogr,2010,57:2002-2007
23 Chen H,Cai L L,Jiao N Z,et al.Viruses in the deep biosphere:A review(in Chinese).Chin Sci Bull,2018,63:3911-3919[陈虹,蔡兰兰,焦念志,等.深部生物圈病毒研究进展与展望.科学通报,2018,63:3911-3919]
24 Engelhardt T,Sahlberg M,Cypionka H,et al.Induction of prophages from deep-subseafloor bacteria.Environ Micro Biol Rep,2011,3:459-465
25 Nigro O D,Jungbluth S P,Lin H T,et al.Viruses in the oceanic basement.m Bio,2017,8:e02129
26 Angly F E,Felts B,Breitbart M,et al.The marine viromes of four oceanic regions.PLo S Biol,2006,4:e368
27 Mizuno C M,Ghai R,Sagha?A,et al.Genomes of abundant and widespread viruses from the deep ocean.m Bio,2016,7:e00805-16
28 Engelhardt T,Kallmeyer J,Cypionka H,et al.High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments.ISMEJ,2014,8:1503-1509
29 Corinaldesi C,Tangherlini M,Dell’Anno A.From virus isolation to metagenome generation for investigating viral diversity in deep-sea sediments.Sci Rep,2017,7:8355
30 Engelhardt T,Orsi W D,J?rgensen B B.Viral activities and life cycles in deep subseafloor sediments.Environ Micro Biol Rep,2015,7:868-873
31 Li Y,Luo T,Sun J,et al.Lytic viral infection of bacterioplankton in deep waters of the western Pacific Ocean.Biogeosciences,2014,11:2531-2542
32 Yang Y,Yokokawa T,Motegi C,et al.Large-scale distribution of viruses in deep waters of the Pacific and Southern Oceans.Aquat Microb Ecol,2014,71:193-202
33 De Corte D,Sintes E,Yokokawa T,et al.Links between viruses and prokaryotes throughout the water column along a North Atlantic latitudinal transect.ISME J,2012,6:1566-1577
34 Lara E,VaquéD,SàE L,et al.Unveiling the role and life strategies of viruses from the surface to the dark ocean.Sci Adv,2017,3:e1602565
35 Magiopoulos I,Pitta P.Viruses in a deep oligotrophic sea:Seasonal distribution of marine viruses in the epi-,meso-and bathypelagic waters of the Eastern Mediterranean Sea.Deep Sea Res Part I-Oceanogr Res Pap,2012,66:1-10
36 Gong Z,Liang Y,Wang M,et al.Viral diversity and its relationship with environmental factors at the surface and deep sea of Prydz Bay,Antarctica.Front Microbiol,2018,9:2981
37 Danovaro R,Corinaldesi C,Dell’anno A,et al.Marine viruses and global climate change.FEMS Microbiol Rev,2011,35:993-1034
38 Chow C E T,Suttle C A.Biogeography of viruses in the sea.Annu Rev Virol,2015,2:41-66
39 Mojica K D A,Brussaard C P D.Factors affecting virus dynamics and microbial host-virus interactions in marine environments.FEMS Microbiol Ecol,2014,89:495-515
40 Johnson R M.Characteristics of a marine Vibrio-bacteriophage system.J Arizona Acad Sci,1968,5:28-33
41 Yoshida M,Yoshida-Takashima Y,Nunoura T,et al.Genomic characterization of a temperate phage of the psychrotolerant deep-sea bacterium Aurantimonas sp..Extremophiles,2015,19:49-58
42 Wang Y,Zhang X.Genome analysis of deep-sea thermophilic phage D6e.Appl Environ Micro Biol,2010,76:7861-7866
43 Yoshida M,Yoshida-Takashima Y,Nunoura T,et al.Identification and genomic analysis of temperate Pseudomonas bacteriophage Pst S-1 from the Japan trench at a depth of 7000 m.Res Microbiol,2015,166:668-676
44 Tang K,Lin D,Zheng Q,et al.Genomic,proteomic and bioinformatic analysis of two temperate phages in Roseobacter clade bacteria isolated from the deep-sea water.BMC Genomics,2017,18:485
45 Liu B,Wu S,Song Q,et al.Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields.Curr Microbiol,2006,53:163-166
46 Liu B,Zhang X.Deep-sea thermophilic Geobacillus bacteriophage GVE2 transcriptional profile and proteomic characterization of virions.Appl Microbiol Biotechnol,2008,80:697-707
47 Lossouarn J,Nesb?C L,Mercier C,et al.‘Ménageàtrois’:A selfish genetic element uses a virus to propagate within Thermotogales.Environ Microbiol,2015,17:3278-3288
48 Mercier C,Lossouarn J,Nesb?C L,et al.Two viruses,MCV1 and MCV2,which infect Marinitoga bacteria isolated from deep-sea hydrothermal vents:Functional and genomic analysis.Environ Microbiol,2018,20:577-587
49 Yoshida-Takashima Y,Takaki Y,Shimamura S,et al.Genome sequence of a novel deep-sea vent epsilonproteobacterial phage provides new insight into the co-evolution of Epsilonproteobacteria and their phages.Extremophiles,2013,17:405-419
50 Geslin C,Le Romancer M,Erauso G,et al.PAV1,the first virus-like particle isolated from a hyperthermophilic Euryarchaeote,“Pyrococcus abyssi”.J Bacteriology,2003,185:3888-3894
51 Gorlas A,Koonin E V,Bienvenu N,et al.TPV1,the first virus isolated from the hyperthermophilic genus Thermococcus.Environ Micro Biol,2012,14:503-516
52 Wang F,Wang F,Li Q,et al.A novel filamentous phage from the deep-sea bacterium Shewanella piezotolerans WP3 is induced at low temperature.J Bacteriol,2007,189:7151-7153
53 Wang F,Wang J,Jian H,et al.Environmental adaptation:Genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3.PLo S One,2008,3:e1937
54 Jian H,Xu J,Xiao X,et al.Dynamic modulation of DNA replication and gene transcription in deep-sea filamentous phage SW1 in response to changes of host growth and temperature.PLo S One,2012,7:e41578
55 Jian H,Xiong L,Xu G,et al.Long 5′untranslated regions regulate the RNA stability of the deep-sea filamentous phage SW1.Sci Rep,2016,6:21908
56 Jian H,Xiong L,Xu G,et al.Filamentous phage SW1 is active and influences the transcriptome of the host at high-pressure and low-temperature.Environ Micro Biol Rep,2016,8:358-362
57 Engelhardt T,Sahlberg M,Cypionka H,et al.Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments.ISME J,2013,7:199-209
58 Millard A D,Hands-Portman I,Zwirglmaier K.Morphotypes of virus-like particles in two hydrothermal vent fields on the East Scotia Ridge,Antarctica.Bacteriophage,2014,4:e28732
59 Wei D,Zhang X.Identification and characterization of a single-stranded DNA-binding protein from thermophilic bacteriophage GVE2.Virus Genes,2008,36:273-278
60 Wang Y,Zhang X.Characterization of a novel portal protein from deep-sea thermophilic bacteriophage GVE2.Gene,2008,421:61-66
61 Wu S,Liu B,Zhang X.Identification of a tail assembly gene cluster from deep-sea thermophilic bacteriophage GVE2.Virus Genes,2009,38:507-514
62 Song Q,Ye T,Zhang X.Proteins responsible for lysogeny of deep-sea thermophilic bacteriophage GVE2 at high temperature.Gene,2011,479:1-9
63 Jin M,Ye T,Zhang X.Roles of bacteriophage GVE2 endolysin in host lysis at high temperatures.Microbiology,2013,159:1597-1605
64 Jin M,Chen Y,Xu C,et al.The effect of inhibition of host Mre B on the infection of thermophilic phage GVE2 in high temperature environment.Sci Rep,2014,4:4823
65 Dell’Anno A,Corinaldesi C,Danovaro R.Virus decomposition provides an important contribution to benthic deep-sea ecosystem functioning.Proc Natl Acad Sci USA,2015,112:E2014-E2019
66 He T,Li H,Zhang X.Deep-sea hydrothermal vent viruses compensate for microbial metabolism in virus-host interactions.m Bio,2017,8:e00893-17
67 López-Pérez M,Haro-Moreno J M,Gonzalez-Serrano R,et al.Genome diversity of marine phages recovered from Mediterranean metagenomes:Size matters.PLo S Genet,2017,13:e1007018
68 Winter C,Garcia J A L,Weinbauer M G,et al.Comparison of deep-water viromes from the atlantic ocean and the mediterranean sea.PLo S One,2014,9:e100600
69 Hurwitz B L,Sullivan M B.The pacific ocean virome(POV):A marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology.PLo S One,2013,8:e57355
70 Anantharaman K,Duhaime M B,Breier J A,et al.Sulfur oxidation genes in diverse deep-sea viruses.Science,2014,344:757-760
71 Suttle C A.Marine viruses-Major players in the global ecosystem.Nat Rev Microbiol,2007,5:801-812
72 Danovaro R,Dell’Anno A,Corinaldesi C,et al.Virus-mediated archaeal hecatomb in the deep seafloor.Sci Adv,2016,2:e1600492
73 Anderson R E,Sogin M L,Baross J A.Evolutionary strategies of viruses,bacteria and archaea in hydrothermal vent ecosystems revealed through metagenomics.PLo S One,2014,9:e109696
74 Hurwitz B L,Brum J R,Sullivan M B.Depth-stratified functional and taxonomic niche specialization in the‘core’and‘flexible’Pacific Ocean Virome.ISME J,2015,9:472-484
75 Jian H,Xiao X,Wang F.Role of filamentous phage SW1 in regulating the lateral flagella of Shewanella piezotolerans strain WP3 at low temperatures.Appl Environ Microbiol,2013,79:7101-7109
76 Lefkowitz E J,Dempsey D M,Hendrickson R C,et al.Virus taxonomy:The database of the international committee on taxonomy of viruses(ICTV).Nucleic Acids Res,2018,46:D708-D717
77 Hurwitz B L,Hallam S J,Sullivan M B.Metabolic reprogramming by viruses in the sunlit and dark ocean.Genome Biol,2013,14:R123
78 Rastelli E,Dell’Anno A,Corinaldesi C,et al.Quantification of viral and prokaryotic production rates in benthic ecosystems:A methods comparison.Front Microbiol,2016,7:1501
79 Tangherlini M,Dell’Anno A,Zeigler Allen L,et al.Assessing viral taxonomic composition in benthic marine ecosystems:Reliability and efficiency of different bioinformatic tools for viral metagenomic analyses.Sci Rep,2016,6:28428
80 Roux S,Brum J R,Dutilh B E,et al.Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses.Nature,2016,537:689-693
81 Orcutt B N,Sylvan J B,Knab N J,et al.Microbial ecology of the dark ocean above,at,and below the seafloor.Micro Biol Mol Biol Rev,2011,75:361-422
82 Zhang R,Wei W,Cai L.The fate and biogeochemical cycling of viral elements.Nat Rev Microbiol,2014,12:850-851
83 Corinaldesi C.New perspectives in benthic deep-sea microbial ecology.Front Mar Sci,2015,2:17
2 Bergh O,B?rsheim K Y,Bratbak G,et al.High abundance of viruses found in aquatic environments.Nature,1989,340:467-468
3 Fuhrman J A.Marine viruses and their biogeochemical and ecological effects.Nature,1999,399:541-548
4 Suttle C A.Viruses in the sea.Nature,2005,437:356-361
5 Wilhelm S W,Suttle C A.Viruses and nutrient cycles in the sea.Bio Science,1999,49:781-788
6 Breitbart M,Bonnain C,Malki K,et al.Phage puppet masters of the marine microbial realm.Nat Microbiol,2018,3:754-766
7 Lu L F,Zhang R,Xu J,et al.Influence of virus upon the marine bacterial metabolism and its biogeochemical effects(in Chinese).Adv Ear Sci,2018,33:225-235[卢龙飞,张锐,徐杰,等.病毒对海洋细菌代谢的影响及其生物地球化学效应.地球科学进展,2018,33:225-235]
8 Wang H,Bai S J,Cai W W,et al.Modulating marine ecosystem by marine viruses-A review(in Chinese).Acta Microbiol Sin,2009,49:551-559[王慧,柏仕杰,蔡雯蔚,等.海洋病毒-海洋生态系统结构与功能的重要调控者.微生物学报,2009,49:551-559]
9 Li S K,Li C B.The progress of the effects of ocean virus on microbial community composition and biogeochemical cycles(in Chinese).Mar Sci,2013,37:117-121[李升康,李传标.海洋病毒在海洋微生物群落及生物地球化学循环中的作用研究进展.海洋科学,2013,37:117-121]
10 Zhang Y Y,Huang C X,Yang J,et al.Interactions between marine microorganisms and their phages.Chin Sci Bull,2011,56:1770-1777
11 Gage J D,Tyler P A.Deep-sea Biology:A Natural History of Organisms at the Deep-Sea Floor.Cambridge:Cambridge University Press,1992
12 Whitman W B,Coleman D C,Wiebe W J.Prokaryotes:The unseen majority.Proc Natl Acad Sci USA,1998,95:6578-6583
13 Hara S,Koike I,Terauchi K,et al.Abundance of viruses in deep oceanic waters.Mar Ecol Prog Ser,1996,145:269-277
14 Magagnini M,Corinaldesi C,Monticelli L S,et al.Viral abundance and distribution in mesopelagic and bathypelagic waters of the Mediterranean Sea.Deep Sea Res Part I-Oceanogr Res Pap,2007,54:1209-1220
15 Arístegui J,Gasol J M,Duarte C M,et al.Microbial oceanography of the dark ocean’s pelagic realm.Limnol Oceanogr,2009,54:1501-1529
16 Nunoura T,Takaki Y,Hirai M,et al.Hadal biosphere:Insight into the microbial ecosystem in the deepest ocean on earth.Proc Natl Acad Sci USA,2015,112:E1230-E1236
17 Danovaro R,Serresi M.Viral density and virus-to-bacterium ratio in deep-sea sediments of the Eastern Mediterranean.Appl Environ Micro Biol,2000,66:1857-1861
18 Danovaro R,Dell’Anno A,Corinaldesi C,et al.Major viral impact on the functioning of benthic deep-sea ecosystems.Nature,2008,454:1084-1087
19 Yoshida M,Takaki Y,Eitoku M,et al.Metagenomic analysis of viral communities in(hado)pelagic sediments.PLo S One,2013,8:e57271
20 Ortmann A C,Suttle C A.High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality.Deep Sea Res Part I-Oceanogr Res Pap,2005,52:1515-1527
21 Ray J,Dondrup M,Modha S,et al.Finding a needle in the virus metagenome haystack-Micro-metagenome analysis captures a snapshot of the diversity of a bacteriophage armoire.PLo S One,2012,7:e34238
22 Kellogg C A.Enumeration of viruses and prokaryotes in deep-sea sediments and cold seeps of the Gulf of Mexico.Deep Sea Res Part II-Topical Stud Oceanogr,2010,57:2002-2007
23 Chen H,Cai L L,Jiao N Z,et al.Viruses in the deep biosphere:A review(in Chinese).Chin Sci Bull,2018,63:3911-3919[陈虹,蔡兰兰,焦念志,等.深部生物圈病毒研究进展与展望.科学通报,2018,63:3911-3919]
24 Engelhardt T,Sahlberg M,Cypionka H,et al.Induction of prophages from deep-subseafloor bacteria.Environ Micro Biol Rep,2011,3:459-465
25 Nigro O D,Jungbluth S P,Lin H T,et al.Viruses in the oceanic basement.m Bio,2017,8:e02129
26 Angly F E,Felts B,Breitbart M,et al.The marine viromes of four oceanic regions.PLo S Biol,2006,4:e368
27 Mizuno C M,Ghai R,Sagha?A,et al.Genomes of abundant and widespread viruses from the deep ocean.m Bio,2016,7:e00805-16
28 Engelhardt T,Kallmeyer J,Cypionka H,et al.High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments.ISMEJ,2014,8:1503-1509
29 Corinaldesi C,Tangherlini M,Dell’Anno A.From virus isolation to metagenome generation for investigating viral diversity in deep-sea sediments.Sci Rep,2017,7:8355
30 Engelhardt T,Orsi W D,J?rgensen B B.Viral activities and life cycles in deep subseafloor sediments.Environ Micro Biol Rep,2015,7:868-873
31 Li Y,Luo T,Sun J,et al.Lytic viral infection of bacterioplankton in deep waters of the western Pacific Ocean.Biogeosciences,2014,11:2531-2542
32 Yang Y,Yokokawa T,Motegi C,et al.Large-scale distribution of viruses in deep waters of the Pacific and Southern Oceans.Aquat Microb Ecol,2014,71:193-202
33 De Corte D,Sintes E,Yokokawa T,et al.Links between viruses and prokaryotes throughout the water column along a North Atlantic latitudinal transect.ISME J,2012,6:1566-1577
34 Lara E,VaquéD,SàE L,et al.Unveiling the role and life strategies of viruses from the surface to the dark ocean.Sci Adv,2017,3:e1602565
35 Magiopoulos I,Pitta P.Viruses in a deep oligotrophic sea:Seasonal distribution of marine viruses in the epi-,meso-and bathypelagic waters of the Eastern Mediterranean Sea.Deep Sea Res Part I-Oceanogr Res Pap,2012,66:1-10
36 Gong Z,Liang Y,Wang M,et al.Viral diversity and its relationship with environmental factors at the surface and deep sea of Prydz Bay,Antarctica.Front Microbiol,2018,9:2981
37 Danovaro R,Corinaldesi C,Dell’anno A,et al.Marine viruses and global climate change.FEMS Microbiol Rev,2011,35:993-1034
38 Chow C E T,Suttle C A.Biogeography of viruses in the sea.Annu Rev Virol,2015,2:41-66
39 Mojica K D A,Brussaard C P D.Factors affecting virus dynamics and microbial host-virus interactions in marine environments.FEMS Microbiol Ecol,2014,89:495-515
40 Johnson R M.Characteristics of a marine Vibrio-bacteriophage system.J Arizona Acad Sci,1968,5:28-33
41 Yoshida M,Yoshida-Takashima Y,Nunoura T,et al.Genomic characterization of a temperate phage of the psychrotolerant deep-sea bacterium Aurantimonas sp..Extremophiles,2015,19:49-58
42 Wang Y,Zhang X.Genome analysis of deep-sea thermophilic phage D6e.Appl Environ Micro Biol,2010,76:7861-7866
43 Yoshida M,Yoshida-Takashima Y,Nunoura T,et al.Identification and genomic analysis of temperate Pseudomonas bacteriophage Pst S-1 from the Japan trench at a depth of 7000 m.Res Microbiol,2015,166:668-676
44 Tang K,Lin D,Zheng Q,et al.Genomic,proteomic and bioinformatic analysis of two temperate phages in Roseobacter clade bacteria isolated from the deep-sea water.BMC Genomics,2017,18:485
45 Liu B,Wu S,Song Q,et al.Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields.Curr Microbiol,2006,53:163-166
46 Liu B,Zhang X.Deep-sea thermophilic Geobacillus bacteriophage GVE2 transcriptional profile and proteomic characterization of virions.Appl Microbiol Biotechnol,2008,80:697-707
47 Lossouarn J,Nesb?C L,Mercier C,et al.‘Ménageàtrois’:A selfish genetic element uses a virus to propagate within Thermotogales.Environ Microbiol,2015,17:3278-3288
48 Mercier C,Lossouarn J,Nesb?C L,et al.Two viruses,MCV1 and MCV2,which infect Marinitoga bacteria isolated from deep-sea hydrothermal vents:Functional and genomic analysis.Environ Microbiol,2018,20:577-587
49 Yoshida-Takashima Y,Takaki Y,Shimamura S,et al.Genome sequence of a novel deep-sea vent epsilonproteobacterial phage provides new insight into the co-evolution of Epsilonproteobacteria and their phages.Extremophiles,2013,17:405-419
50 Geslin C,Le Romancer M,Erauso G,et al.PAV1,the first virus-like particle isolated from a hyperthermophilic Euryarchaeote,“Pyrococcus abyssi”.J Bacteriology,2003,185:3888-3894
51 Gorlas A,Koonin E V,Bienvenu N,et al.TPV1,the first virus isolated from the hyperthermophilic genus Thermococcus.Environ Micro Biol,2012,14:503-516
52 Wang F,Wang F,Li Q,et al.A novel filamentous phage from the deep-sea bacterium Shewanella piezotolerans WP3 is induced at low temperature.J Bacteriol,2007,189:7151-7153
53 Wang F,Wang J,Jian H,et al.Environmental adaptation:Genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3.PLo S One,2008,3:e1937
54 Jian H,Xu J,Xiao X,et al.Dynamic modulation of DNA replication and gene transcription in deep-sea filamentous phage SW1 in response to changes of host growth and temperature.PLo S One,2012,7:e41578
55 Jian H,Xiong L,Xu G,et al.Long 5′untranslated regions regulate the RNA stability of the deep-sea filamentous phage SW1.Sci Rep,2016,6:21908
56 Jian H,Xiong L,Xu G,et al.Filamentous phage SW1 is active and influences the transcriptome of the host at high-pressure and low-temperature.Environ Micro Biol Rep,2016,8:358-362
57 Engelhardt T,Sahlberg M,Cypionka H,et al.Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments.ISME J,2013,7:199-209
58 Millard A D,Hands-Portman I,Zwirglmaier K.Morphotypes of virus-like particles in two hydrothermal vent fields on the East Scotia Ridge,Antarctica.Bacteriophage,2014,4:e28732
59 Wei D,Zhang X.Identification and characterization of a single-stranded DNA-binding protein from thermophilic bacteriophage GVE2.Virus Genes,2008,36:273-278
60 Wang Y,Zhang X.Characterization of a novel portal protein from deep-sea thermophilic bacteriophage GVE2.Gene,2008,421:61-66
61 Wu S,Liu B,Zhang X.Identification of a tail assembly gene cluster from deep-sea thermophilic bacteriophage GVE2.Virus Genes,2009,38:507-514
62 Song Q,Ye T,Zhang X.Proteins responsible for lysogeny of deep-sea thermophilic bacteriophage GVE2 at high temperature.Gene,2011,479:1-9
63 Jin M,Ye T,Zhang X.Roles of bacteriophage GVE2 endolysin in host lysis at high temperatures.Microbiology,2013,159:1597-1605
64 Jin M,Chen Y,Xu C,et al.The effect of inhibition of host Mre B on the infection of thermophilic phage GVE2 in high temperature environment.Sci Rep,2014,4:4823
65 Dell’Anno A,Corinaldesi C,Danovaro R.Virus decomposition provides an important contribution to benthic deep-sea ecosystem functioning.Proc Natl Acad Sci USA,2015,112:E2014-E2019
66 He T,Li H,Zhang X.Deep-sea hydrothermal vent viruses compensate for microbial metabolism in virus-host interactions.m Bio,2017,8:e00893-17
67 López-Pérez M,Haro-Moreno J M,Gonzalez-Serrano R,et al.Genome diversity of marine phages recovered from Mediterranean metagenomes:Size matters.PLo S Genet,2017,13:e1007018
68 Winter C,Garcia J A L,Weinbauer M G,et al.Comparison of deep-water viromes from the atlantic ocean and the mediterranean sea.PLo S One,2014,9:e100600
69 Hurwitz B L,Sullivan M B.The pacific ocean virome(POV):A marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology.PLo S One,2013,8:e57355
70 Anantharaman K,Duhaime M B,Breier J A,et al.Sulfur oxidation genes in diverse deep-sea viruses.Science,2014,344:757-760
71 Suttle C A.Marine viruses-Major players in the global ecosystem.Nat Rev Microbiol,2007,5:801-812
72 Danovaro R,Dell’Anno A,Corinaldesi C,et al.Virus-mediated archaeal hecatomb in the deep seafloor.Sci Adv,2016,2:e1600492
73 Anderson R E,Sogin M L,Baross J A.Evolutionary strategies of viruses,bacteria and archaea in hydrothermal vent ecosystems revealed through metagenomics.PLo S One,2014,9:e109696
74 Hurwitz B L,Brum J R,Sullivan M B.Depth-stratified functional and taxonomic niche specialization in the‘core’and‘flexible’Pacific Ocean Virome.ISME J,2015,9:472-484
75 Jian H,Xiao X,Wang F.Role of filamentous phage SW1 in regulating the lateral flagella of Shewanella piezotolerans strain WP3 at low temperatures.Appl Environ Microbiol,2013,79:7101-7109
76 Lefkowitz E J,Dempsey D M,Hendrickson R C,et al.Virus taxonomy:The database of the international committee on taxonomy of viruses(ICTV).Nucleic Acids Res,2018,46:D708-D717
77 Hurwitz B L,Hallam S J,Sullivan M B.Metabolic reprogramming by viruses in the sunlit and dark ocean.Genome Biol,2013,14:R123
78 Rastelli E,Dell’Anno A,Corinaldesi C,et al.Quantification of viral and prokaryotic production rates in benthic ecosystems:A methods comparison.Front Microbiol,2016,7:1501
79 Tangherlini M,Dell’Anno A,Zeigler Allen L,et al.Assessing viral taxonomic composition in benthic marine ecosystems:Reliability and efficiency of different bioinformatic tools for viral metagenomic analyses.Sci Rep,2016,6:28428
80 Roux S,Brum J R,Dutilh B E,et al.Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses.Nature,2016,537:689-693
81 Orcutt B N,Sylvan J B,Knab N J,et al.Microbial ecology of the dark ocean above,at,and below the seafloor.Micro Biol Mol Biol Rev,2011,75:361-422
82 Zhang R,Wei W,Cai L.The fate and biogeochemical cycling of viral elements.Nat Rev Microbiol,2014,12:850-851
83 Corinaldesi C.New perspectives in benthic deep-sea microbial ecology.Front Mar Sci,2015,2:17