FULL GENOME RESOURCES for Apis mellifera, its pathosphere and microbiota.

Table S1.  Full genome resources1 for Apis mellifera, its pathosphere and microbiota.
(modified from Schwarz RS, Huang Q, and Evans JE. 2015. Hologenome theory and the honey bee pathosphere.  Current Opinion in Insect Science. doi:10.1016/j.cois.2015.04.006)

Taxon and isolate
GenBank accession
Location
Reference
PATHOSPHERE
Viruses
Iflaviridae



DWV IT
DWV PA
DWV Ox
DWV Korea-1
DWV Korea-2
DWV DJE202
DWV Warwick-2009
Italy
USA
UK
S Korea
S Korea
UK
UK
[1]
[1]
[2]
[3]
[3]
[4]
[4]
DWV Kakugo
DWV KV-like Ox
Japan
UK
[5]
[2]
SBPV Rothamsted
SBPV Harpenden
UK
UK
[6]
[6]
SBV Rothamsted
SBV CSBV-GZ
SBV CSBV-LN
SBV Kor19
SBV Kor21
SBV Oksapmin
SBV AmSBV-Viet4
SBV AmSBV-Viet6
UK
China
China
S Korea
S Korea
PNG
Vietnam
Vietnam
[7]
[8]
[9]
[10]
[10]
[11]
unpublished
unpublished
VDV-12,3
VDV-1 Zriffin
VDV-1 Ox
Netherlands
Israel
UK
[12]
[13]
[2]
Dicistroviridae



ABPV Rothamsted
ABPV Poland 1
ABPV Hungary 1
UK
Poland
Hungary
[14]
[15]
[15]
BQCV SA
BQCV Poland-4
BQCV Poland-5
BQCV Poland-6
BQCV Hungary-10
BQCV AY
BQCV JL1
S Africa
Poland
Poland
Poland
Hungary
S Korea
China
[16]
[17]
[17]
[17]
[17]
[18]
unpublished
IAPV
IAPV CA
IAPV MD
IAPV PA
IAPV DVE31-OP3-PA-USA-2007
IAPV IS1-ISRAEL-2007
IAPV OZ6-AUSTRALIA-2007
IAPV Wus-China-2008
IAPV Korea1
IAPV Korea2
IAPV Korea3
IAPV 4782IAPV
Israel
USA
USA
USA
USA
Israel
Australia
China
S Korea
S Korea
S Korea
Spain
[19]
[20]
[20]
[20]
[21]
[21]
[21]
unpublished
[22]
[22]
[22]
[23]
KBV PA
KBV AY
USA
S Korea
[24]
[25]
Unclassified



CBPV A-79P

CBPV B-441
France

France
[26]

[26]
LSV-1 BruceSD_T17E02
LSV-2 BruceSD_T17E01
USA
USA
[27]
[27]
Bacteria
Firmicutes



Melissococcus plutonius ATCC 35311

Melissococcus plutonius DAT561

APO12200 (chr)
AP012201 (pld)
AP012282 (chr)
AP012283 (pld)
UK

Japan

[28]

[29]

Paenibacillus larvae BRL-230010
Paenibacillus larvae DSM 25719 (ERIC I)
Paenibacillus larvae DSM 25430 (ERIC II)
CP003355 (chr)
CP003356 (pld)
USA
Germany

Germany

[30]
[31]

[31]

Tenericutes



Spiroplasma apis B31T
France
[32]
Spiroplasma melliferum KC3
Spiroplasma melliferum IPMB4A
France
Taiwan
[33]
[34]
Fungi
Ascomycota



Ascosphaera apis USDA-ARSEF 7405
USA
[30]
Aspergillus flavus NRRL33575
USA
[35]
Microsporidia



Nosema apis BRL01
Canada
[36]
Nosema ceranae BRL01
USA
[37]
Protists
Euglenozoa



Lotmaria passim SF6
USA
[38]
Metazoa
Arthropoda



Varroa destructor Korean
Varroa destructor Korean
Varroa destructor Korean
AY163547 (mtd)
NC_004454 (mtd)
USA
USA
France
[39]
[40]
[41]












MICROBIOTA
Actinobacteria



Bifidobacterium asteroides PRL2011
Bifidobacterium asteroides DSM20098

Bifidobacterium asteroides Bin2
Bifidobacterium asteroides Bin7
CP003325 (chr)
NC_010908 (pld)
Italy
Italy
Italy
Sweden
Sweden
[42]
[43]
[44]
unpublished
unpublished
Firmicutes



Lactobacillus
helsingborgensis wkB8
Lactobacillus
helsingborgensis Bma5
CP009531 (chr)
CP009532 (pld)
PRJNA257138 7 (gen)
USA

Sweden
[45]

[46]
Lactobacillus kimbladii Hma2
PRJNA257141 7 (gen)
Sweden
[46]
Lactobacillus kullabergensis Biut2
Sweden
[46]
Lactobacillus kunkeei MP2
Lactobacillus kunkeei EFB6
Lactobacillus kunkeei AR114
Chile
Germany
Norway
[47]
[48]
[49]
Lactobacillus mellifer Bin4
PRJNA257185 7 (gen)
Sweden
[46]
Lactobacillus mellis Hon2
Sweden
[46]
Lactobacillus melliventris Hma8
PRJNA257139 7 (gen)
Sweden
[46]
Lactobacillus sp. wkB10
USA
[45]
Proteobacteria



Frischella perrara PEB0191
CP009056 (gen)
USA
[50]
Gilliamella apicola wkB1T
CP007445 (chr)
USA
[51]
Snodgrassella alvi wkB2T
CP007446 (chr)
USA
[51]




HONEY BEE HOST
Apis mellifera ligustica DH4 hybrid
USA
[52,53]
Taxa are organized by Family (viruses) or Phylum.  ABPV: Acute bee paralysis virus, BQCV: Black queen cell virus, CBPV: Chronic bee paralysis virus, chr: chromosome, DWV: Deformed wing virus, gen: whole genome, KBV: Kashmir bee virus, KV: Kakugo virus, LSV: Lake Sinai virus, mtd: mitochondria, pld: plasmid, PNG: Papua New Guinea, SBPV: Slow bee paralysis virus, SBV: Sacbrood virus, UK: United Kingdom, USA: United States of America, VDV-1: Varroa destructor virus-1.
(1) As of 01 April 2015.
(2) Obtained from Varroa destructor mite but is also infectious to A. mellifera.
(3) Recombinant DWV/VDV genomes were not included.
(4) RNA 1 and RNA 2 genomes, respectively.
(5) Not a honey bee isolate, but present in A. mellifera per [54].
(6) Originally accessioned as Crithidia mellificae but renamed in [55].
(7) BioProject accession: at publication, only unassembled sequence reads were available. 

References
1.        Lanzi G, Miranda JR De, Boniotti MB, Cameron CE, Lavazza A, Capucci L, Camazine SM, Rossi C: Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L .). J Virol 2006, 80:4998–5009.
2.        Wang H, Xie J, Shreeve TG, Ma J, Pallett DW, King LA, Possee RD: Sequence Recombination and Conservation of Varroa destructor Virus-1 and Deformed Wing Virus in Field Collected Honey Bees (Apis mellifera). PLoS One 2013, 8:1–9.
3.        Reddy KE, Noh JH, Yoo MS, Kim YH, Kim NH, Doan HTT, Ramya M, Jung SC, Van Quyen D, Kang SW: Molecular characterization and phylogenetic analysis of deformed wing viruses isolated from South Korea. Vet Microbiol 2013, 167:272–279.
4.        Ryabov E V., Wood GR, Fannon JM, Moore JD, Bull JC, Chandler D, Mead A, Burroughs N, Evans DJ: A Virulent Strain of Deformed Wing Virus (DWV) of Honeybees (Apis mellifera) Prevails after Varroa destructor-Mediated, or In Vitro, Transmission. PLoS Pathog 2014, 10.
5.        Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto a., Kubo T: Novel Insect Picorna-Like Virus Identified in the Brains of Aggressive Worker Honeybees. J Virol 2004, 78:1093–1100.
6.        De Miranda JR, Dainat B, Locke B, Cordoni G, Berthoud H, Gauthier L, Neumann P, Budge GE, Ball B V., Stoltz DB: Genetic characterization of slow bee paralysis virus of the honeybee (Apis mellifera L.). J Gen Virol 2010, 91:2524–2530.
7.        Ghosh RC, Ball B V., Willcocks MM, Carter MJ: The nucleotide sequence of sacbrood virus of the honey bee: An insect picorna-like virus. J Gen Virol 1999, 80:1541–1549.
8.        Zhang J, Feng J, Liang Y, Chen D, Zhou ZH, Zhang Q, Lu X: Three-dimensional structure of the Chinese Sacbrood bee virus. Sci China C Life Sci 2001, 44:443–448.
9.        Ma M, Ma C, Li M, Wang S, Yang S, Wang S: Loop-mediated isothermal amplification for rapid detection of Chinese sacbrood virus. J Virol Methods 2011, 176:115–119.
10.      Choe SE, Nguyen LTK, Noh JH, Kweon CH, Reddy KE, Koh HB, Chang KY, Kang SW: Analysis of the complete genome sequence of two Korean sacbrood viruses in the Honey bee, Apis mellifera. Virology 2012, 432:155–161.
11.      Roberts JMK, Anderson DL: A novel strain of sacbrood virus of interest to world apiculture. J Invertebr Pathol 2014, 118:71–4.
12.      Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers MM: Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol 2004, 85:3747–3755.
13.      Zioni N, Soroker V, Chejanovsky N: Replication of varroa destructor virus 1 (VDV-1) and a varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology 2011, 417:106–112.
14.      Govan V a, Leat N, Allsopp M, Davison S: Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology 2000, 277:457–463.
15.      Bakonyi T, Grabensteiner E, Kolodziejek J, Rusvai M, Topolska G, Ritter W, Nowotny N: Phylogenetic Analysis of Acute Bee Paralysis Virus Strains Phylogenetic Analysis of Acute Bee Paralysis Virus Strains. 2002, 68:6446–6450.
16.      Leat N, Ball B, Govan V, Davison S: Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honey bees. J Gen Virol 2000, 81:2111–2119.
17.      Tapaszti Z, Forgách P, Kovágó C, Topolska G, Nowotny N, Rusvai M, Bakonyi T: Genetic analysis and phylogenetic comparison of Black queen cell virus genotypes. Vet Microbiol 2009, 139:227–234.
18.      Reddy KE, Noh JH, Choe SE, Kweon CH, Yoo MS, Doan HTT, Ramya M, Yoon BS, Nguyen LTK, Nguyen TTD, et al.: Analysis of the complete genome sequence and capsid region of black queen cell viruses from infected honeybees (Apis mellifera) in Korea. Virus Genes 2013, 47:126–132.
19.      Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I: Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: Evidence for diversity due to intra- and inter-species recombination. J Gen Virol 2007, 88:3428–3438.
20.      Chen YP, Pettis JS, Corona M, Chen WP, Li CJ, Spivak M, Visscher PK, DeGrandi-Hoffman G, Boncristiani H, Zhao Y, et al.: Israeli Acute Paralysis Virus: Epidemiology, Pathogenesis and Implications for Honey Bee Health. PLoS Pathog 2014, 10.
21.      Palacios G, Hui J, Quan PL, Kalkstein a, Honkavuori KS, Bussetti a V, Conlan S, Evans J, Chen YP, vanEngelsdorp D, et al.: Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol 2008, 82:6209–6217.
22.      Reddy KE, Noh JH, Kim YH, Yoo MS, Doan HTT, Ramya M, Jung SC, Quyen D Van, Kang SW: Analysis of the nonstructural and structural polyprotein regions, and complete genome sequences of Israel acute paralysis viruses identified from honeybees (Apis mellifera) in Korea. Virology 2013, 444:211–217.
23.      Granberg F, Vicente-Rubiano M, Rubio-Guerri C, Karlsson OE, Kukielka D, Belák S, Sánchez-Vizcaíno JM: Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses. PLoS One 2013, 8.
24.      De Miranda JR, Drebot M, Tyler S, Shen M, Cameron CE, Stoltz DB, Camazine SM: Complete nucleotide sequence of Kashmir bee virus and comparison with acute bee paralysis virus. J Gen Virol 2004, 85:2263–2270.
25.      Reddy KE, Yoo MS, Kim YH, Kim NH, Jung HN, Thao LTB, Ramya M, Doan HTT, Nguyen LTK, Jung SC, et al.: Analysis of the RdRp, intergenic and structural polyprotein regions, and the complete genome sequence of Kashmir bee virus from infected honeybees (Apis mellifera) in Korea. Virus Genes 2014, 49:137–144.
26.      Olivier V, Blanchard P, Chaouch S, Lallemand P, Schurr F, Celle O, Dubois E, Tordo N, Thiéry R, Houlgatte R, et al.: Molecular characterisation and phylogenetic analysis of Chronic bee paralysis virus, a honey bee virus. Virus Res 2008, 132:59–68.
27.      Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, Andino R, DeRisi JL: Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 2011, 6:e20656.
28.      Okumura K, Arai R, Okura M, Kirikae T, Takamatsu D, Osaki M, Miyoshi-Akiyama T: Complete genome sequence of Melissococcus plutonius ATCC 35311. J Bacteriol 2011, 193:4029–4030.
29.      Okumura K, Arai R, Okura M, Kirikae T, Takamatsu D, Osaki M, Miyoshi-Akiyama T: Complete genome sequence of melissococcus plutonius DAT561, a strain that shows an unusual growth profile and is representative of an endemic cluster in japan. J Bacteriol 2012, 194:3014.
30.      Qin X, Evans JD, Aronstein K a., Murray KD, Weinstock GM: Genome sequences of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Mol Biol 2006, 15:715–718.
31.      Djukic M, Brzuszkiewicz E, Fünfhaus A, Voss J, Gollnow K, Poppinga L, Liesegang H, Garcia-Gonzalez E, Genersch E, Daniel R: How to kill the honey bee larva: Genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS One 2014, 9.
32.      Ku C, Lo W-S, Chen L-L, Kuo C-H: Complete Genome Sequence of Spiroplasma apis B31 (ATCC 33834), a Bacterium Associated with May Disease of Honeybees (Apis mellifera). Genome Announc 2014, 2:e01151–13.
33.      Alexeev D, Kostrjukova E, Aliper A, Popenko A, Bazaleev N, Tyakht A, Selezneva O, Akopian T, Prichodko E, Kondratov I, et al.: Application of Spiroplasma melliferum proteogenomic profiling for the discovery of virulence factors and pathogenicity mechanisms in host-associated spiroplasmas. J Proteome Res 2012, 11:224–236.
34.      Lo W-S, Chen L-L, Chung W-C, Gasparich GE, Kuo C-H: Comparative genome analysis of Spiroplasma melliferum IPMB4A, a honeybee-associated bacterium. BMC Genomics 2013, 14:22.
35.      Yu J, Cleveland TE, Nierman WC, Bennett JW: Aspergillus flavus genomics: gateway to human and animal health, food safety, and crop resistance to diseases. Rev Iberoam Micol 2005, 22:194–202.
36.      Chen YP, Pettis JS, Zhao Y, Liu X, Tallon LJ, Sadzewicz LD, Li R, Zheng H, Huang S, Zhang X, et al.: Genome sequencing and comparative genomics of honey bee microsporidia, Nosema apis reveal novel insights into host-parasite interactions. BMC Genomics 2013, 14:451.
37.      Cornman RS, Chen YP, Schatz MC, Street C, Zhao Y, Desany B, Egholm M, Hutchison S, Pettis JS, Lipkin WI, et al.: Genomic Analyses of the Microsporidian Nosema ceranae, an Emergent Pathogen of Honey Bees. PLoS Pathog 2009, 5:e1000466.
38.      Runckel C, Derisi J, Flenniken ML: A Draft Genome of the Honey Bee Trypanosomatid Parasite Crithidia mellificae. PLoS One 2014, 9:e95057.
39.      Cornman SR, Schatz MC, Johnston SJ, Chen Y-P, Pettis J, Hunt G, Bourgeois L, Elsik C, Anderson D, Grozinger CM, et al.: Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 2010, 11:602.
40.      Evans JD, Lopez DL: Complete mitochondrial DNA sequence of the important honey bee pest , Varroa destructor (Acari: Varroidae). Exp Appl Acarol 2002, 27:69–78.
41.      Navajas M, Le Conte Y, Solignac M, Cros-Arteil S, Cornuet J-M: The Complete Sequence of the Mitochondrial Genome of the Honeybee Ectoparasite Mite Varroa destructor (Acari: Mesostigmata). Mol Biol Evol 2002, 19:2313–2317.
42.      Bottacini F, Milani C, Turroni F, Sánchez B, Foroni E, Duranti S, Serafini F, Viappiani A, Strati F, Ferrarini A, et al.: Bifidobacterium asteroides PRL2011 Genome Analysis Reveals Clues for Colonization of the Insect Gut. PLoS One 2012, 7:1–14.
43.      Sun Z, Zhang W, Guo C, Yang X, Liu W, Wu Y, Song Y, Kwok LY, Cui Y, Menghe B, et al.: Comparative Genomic Analysis of 45 Type Strains of the Genus Bifidobacterium: A Snapshot of Its Genetic Diversity and Evolution. PLoS One 2015, 10:e0117912.
44.      Cronin M, Knobel M, O’Connell-Motherway M, Fitzgerald GF, Van Sinderen D: Molecular dissection of a bifidobacterial replicon. Appl Environ Microbiol 2007, 73:7858–7866.
45.      Kwong WK, Mancenido AL, Moran A: Genome sequences of Lactobacillus sp. strains wkB8 and wkB10, members of the Firm-5 clade, from honey bee guts. Genome Announc 2014, 2:e01176–14.
46.      Olofsson TC, Alsterfjord M, Nilson B, Butler E, Vásquez A: Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov., and Lactobacillus kullabergensis sp. nov., iso. Int J Syst Evol Microbiol 2014, doi:10.1099/ijs.0.059600-0.
47.      Olmos A, Henríquez-piskulich P, Sanchez C, Rojas-herrera M, Moreno-pino M, Gómez M, Rodríguez R, Silva D, Maracaja-coutinho V, Aldea P, et al.: Draft Genome of Chilean Honeybee ( Apis mellifera ) Gut Strain Lactobacillus kunkeei MP2. 2014, 2:2013–2014.
48.      Djukic M, Poehlein A, Strauß J, Tann F, Leimbach A, Hoppert M, Daniel R: High quality draft genome of Lactobacillus kunkeei EFB6, isolated from a German European foulbrood outbreak of honeybees. Stand Genomic Sci 2015, 10:16.
49.      Porcellato D, Frantzen C, Rangberg A, Umu OC, Gabrielsen C, Nes IF, Amdam G V, Diep DB: Draft Genome Sequence of Lactobacillus kunkeei AR114 Isolated from Honey Bee Gut. Genome Announc 2015, 3:e00144–15.
50.      Engel P, Vizcaino MI, Crawford JM: Gut Symbionts from Distinct Hosts Exhibit Genotoxic Activity via Divergent Colibactin Biosynthesis Pathways. Appl Environ Microbiol 2015, 81:1502–1512.
51.      Kwong WK, Engel P, Koch H, Moran NA: Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc Natl Acad Sci 2014, 111 :11509–11514.
52.      Elsik CG, Worley KC, Bennett AK, Beye M, Camara F, Childers CP, de Graaf DC, Debyser G, Deng J, Devreese B, et al.: Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics 2014, 15:86.
53.      Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R, Robertson HM, Weaver DB, Beye M, Bork P, et al.: Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931–949.
54.      Foley K, Fazio G, Jensen AB, Hughes WOH: The distribution of Aspergillus spp. opportunistic parasites in hives and their pathogenicity to honey bees. Vet Microbiol 2014, 169:203–210.
55.      Schwarz RS, Bauchan GR, Murphy CA, Ravoet J, de Graaf DC, Evans JD: Characterization of Two Species of Trypanosomatidae from the Honey Bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim n. gen., n. sp. J Eukaryot Microbiol 2015, doi:10.1111/jeu.12209.


1 comment:

  1. To keep this up-to-date, please send me a message if you have additional or updated genomic resources that should be posted here.

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