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A'&'=A:;M '! viii TABLE OF CONTENTS LIST OF TABLES ........................................................................................................... xi LIST OF FI GURES ....................................................................................................... xiii CHAPTER 1 ...................................................................................................................... 1 INTRODUCTION ............................................................................................................ 1 1.1. Bioinvasion through ballast water ........................................................................... 2 1.2. Status of ballast water management guidelines and standards ................................ 3 1.3. Knowledge gaps in the curr ent understanding of viruses in ballast water ............... 6 1.4. Dissertation outline .................................................................................................. 6 REFERENCES ............................................................................................................... 8 CHAPTER 2 .................................................................................................................... 12 LITERATURE REVIEW .............................................................................................. 12 2.1. Overview ................................................................................................................ 13 2.2. Occurrence of viruses in ballast water ................................................................... 13 2.3. Methods for the detection of viruses in aquatic environments .............................. 17 2.3.1. Electron microscopy ....................................................................................... 17 2.3.2. Cell culture ...................................................................................................... 17 2.3.3. Polymerase chain reaction (PCR) ................................................................... 18 2.3.4. Metagenomics ................................................................................................. 19 2.4. Application of metagenomics to study virus es in aquatic environments ............... 21 2.5. Methods used to prepare viromes in aquatic environments ................................... 27 2.6. Summary of literature review ................................................................................ 33 REFERENCES ............................................................................................................. 34 CHAPTER 3 .................................................................................................................... 41 RESEARCH QUESTIONS AND OBJECTIVES ........................................................ 41 CHAPTER 4 .................................................................................................................... 44 MATERIALS AND METHODS ................................................................................... 44 4.1. Overview ................................................................................................................ 45 4.2. Evaluation and optimization of sample preparation methods ................................ 45 4.2.1. Evaluation of the tangential flow filtration method using groundwater and surface water ............................................................................................................. 45 4.2.1.1. Tangential flow filtration setup and procedure ........................................ 45 4.2.1.2. Data analysis and statistics ....................................................................... 49 4.2.1.3. Virus recovery by tangential flow filtration ............................................. 50 4.2.2. Evaluation of nucleic acid extraction methods for simultaneous recovery of viral DNA and RNA ................................................................................................. 53 4.2.2.1. Standard curve generation for quantitative PCR assay ............................ 53 ix 4.2.2.2. Viral nucleic acid extraction and quantitative PCR detection ................. 58 4.2.2.3. Data analysis an d statistics ....................................................................... 58 4.2.2.4. Comparison of viral nucleic acid extraction methods .............................. 59 4.3. Description of materials and methods used for preparing and analyzing viromes 62 4.3.1. Viro me preparation ......................................................................................... 64 4.3.1.1. Sample collection ..................................................................................... 64 4.3.1.2. Variable measurement and estimation ..................................................... 64 4.3.1.3. Primary concentration of viral particles ................................................... 65 4.3.1.4. Secondary concentration of viral particles ............................................... 65 4.3.1.5. Pu rification of viral particles ................................................................... 65 4.3.1.6. Viral nucleic acid extraction .................................................................... 66 4.3.1.7. Random transcription/amplification of viral nucleic acid extracts .......... 66 4.3.2. High !through put sequencing .......................................................................... 68 4.3.3. Bioinformatics analyses .................................................................................. 68 4.3.3.1. Preproce ssing and quality control of raw sequence reads ....................... 68 4.3.3.2. De novo assembly of sequence reads ....................................................... 69 4.3.3.3. Taxonomic classification ......................................................................... 69 REFERENCES ............................................................................................................. 72 CHAPTER 5 .................................................................................................................... 75 METAGENOMIC INVESTIGATION OF BALLAST WATER VIRAL COMMUNITIES IN THE GREAT LAKES ................................................................ 75 Abstract ......................................................................................................................... 76 5.1. Introduction ............................................................................................................ 77 5.2. Materials and methods ........................................................................................... 80 5.2.1. Sample collection ............................................................................................ 80 5.2.2. Preparation and sequencing of viromes .......................................................... 85 5.2.3. Analysis of viromes ........................................................................................ 85 5.2.4. Data access ...................................................................................................... 86 5.3. Results .................................................................................................................... 87 5.3.1. General water quality ...................................................................................... 87 5.3.2. Overview of the virome data sets .................................................................... 89 5.3.3. Taxonomic profile of the Great Lakes ballast and harbor water viromes ....... 92 5.3.4. Viral pathogens of fish and shrimp in the Great Lakes ballast and harbor waters ...................................................................................................................... 107 5.3.5. Comparison among the Great Lakes ballast and harbor water viromes ....... 112 5.3.6. Comparison of the Great Lakes ballast and harbor water viromes with other aquatic viromes ....................................................................................................... 117 5.4. Discussion ............................................................................................................ 120 5.4.1. Diversity of viruses in ballast water .............................................................. 120 5.4.2. Implications and control of viruses in ballast water ..................................... 123 APPENDIX ................................................................................................................. 127 REFERENCES ........................................................................................................... 129 CHAPTER 6 .................................................................................................................. 136 TRANSPORTING OCEAN VIROMES: INVASION OF THE AQUATIC x BIOSPHERE ................................................................................................................. 136 Abstract ....................................................................................................................... 137 6.1. Introduction .......................................................................................................... 138 6.2. Materials and methods ......................................................................................... 139 6.2.1. Sample collection .......................................................................................... 139 6.2.2. Preparation and sequencing of viromes ........................................................ 145 6.2.3. Analysis of viromes ...................................................................................... 145 6.2.4. Data access .................................................................................................... 146 6.3. Results and discussion ......................................................................................... 147 6.3.1. Influence of global shipping on transport of the ocean virome .................... 147 6.3.2. Effect of engineered, management , and environmental variables on the ocean virome ..................................................................................................................... 165 6.3.3. Potential invasion by rare viral pathogens .................................................... 173 6.4. Conclusions .......................................................................................................... 182 APPENDIX ................................................................................................................. 183 REFERENCES ........................................................................................................... 187 CHAPTER 7 .................................................................................................................. 191 CONCLUSIONS ........................................................................................................... 191 7.1. Summary .............................................................................................................. 192 7.2. Implications for policy and technological development ...................................... 194 7.3. Limitations and recommendations for future research ........................................ 196 REFERENCES ........................................................................................................... 200 xi LIST OF TABLES Table 1.1. Numeric ballast water discharge standards at the federal and state level ......... 5! Table 2.1. Viral levels found in ballast water .................................................................. 15! Table 2.2. Metagenomic studies in aquatic viral ecology ................................................ 24! Table 2.3. Methods used in published studies to prepare viromes from aquatic environments ..................................................................................................................... 28! Table 4.1. Percent recovery efficiencies (average ± standard deviation) of phages in 20 ÐL groundwater and 20 ÐL surface water samples .................................................................. 52! Table 4.2. Sequence of the primers and probes and PCR protocol used for quantitative PCR assay ......................................................................................................................... 55! Table 5.1. Identification, description, and collection information for the ballast and harbor water samples ........................................................................................................ 83! Table 5.2. Water quality of the ballast and harbor water samples ................................... 88! Table 5.3. Summary of virome datasets ........................................................................... 90! Table 5.4. Sample Ðspecific PE reads mapped to individual assemblies .......................... 91! Table 5.5. Distribution of dsDNA phage hosts identified in the ballast and harbor water viromes .............................................................................................................................. 99! Table 5.6. Relative abundance of the viral families in the ballast and harbor water viromes ............................................................................................................................ 104! Table 5.7. Contigs identified as viral pathogens of fish and s hrimp by BLASTX search against the NCBI RefSeq database ................................................................................. 109! Table 5.8. Summary statistics of read mapping to five reference genomes of koi herpesvirus ...................................................................................................................... 110! Table 5.9. Similarity matrix of contigs between ballast and harbor water viromes using TBLASTX ....................................................................................................................... 115! Table 5.10. Similarity matrix of contigs between ballast and harbor water viromes using QUAST ........................................................................................................................... 116! xii Table 5.11. Accession number of the Illumina HiSeq sequencing data ......................... 128! Table 6.1. Summary of sampling information ............................................................... 141! Table 6.2. Summary of engineered, management, and environmental variables ........... 143! Table 6.3. Overview of the sequence reads and the assembled contigs of the virome libraries ........................................................................................................................... 150! Table 6.4. Summary of Similarity Percentage (SIMPER) analysis ............................... 158! Table 6.5. Identified viral pathogens by performing BLASTX searches against non!redundant (nr) d atabase .......................................................................................... 176! Table 6.6. Accession number of the Illumina HiSeq sequencing data ........................... 184! xiii LIST OF FI GURES Figure 4.1. Experimental setup for the tangential flow filtration using ultrafilters with 30,000 Dalton molecular weight cutoff. The retentate is recirculated until the volume remained is less than 500 mL. ........................................................................................... 47! Figure 4.2. A procedure for virus concentration from the groundwater and surface water samples. ............................................................................................................................. 48! Figure 4.3. Standard curve s for the quantification of MS2 cDNA (A) and PhiX174 DNA (B) using the LightCycler Instrument and the LightCycler 480 Probe Master mix. ........ 56! Figure 4.4. Comparison of qPCR C T value for viral nucleic acid extracts from seeded water with 10 5 and 10 6 PFUs/mL of MS2 (A) and PhiX174 (B). The error bars represent standard deviation of the C T value calculated from six replicates. Different letters in the figure indicate si gnificant differences according to Bonferroni LSD multiple comparison tests ( p < 0.05). ................................................................................................................. 60! Figure 4.5. A pipeline for the viral metagenomic study with high Ðthroughput sequencing used in this research. ......................................................................................................... 63! Figure 5.1. Google Earth maps showing the Great Lakes (left) and ballast water source and discharge ports of the five vessels (right). Ballast waters (AB, BB, IB, MB, and PB) were originated from different parts (Lakes Erie, Huron, Michigan, and Ontario) of the Great Lakes but all discharged in three terminals (BH, IH, and MH) of the Port of Duluth ÐSuperior. ............................................................................................................... 82! Figure 6.1. Relative distribution of viromes from ballast and ha rbor waters. Pie charts represent a mean relative abundance of assigned viral families (three replicates from 24 samples). ÔOthersÕ are viral families whose maximum relative abundances across viromes are less than 3% (including RNA viruses). Vessels with b allast waters arriving in the Port of Los Angeles/Long Beach are shown as a green star and the Port of Singapore as a red star. Circles and squares in the map indicate ballast waters exchanged beyond and within 200 nautical miles from nearest shoreline, re spectively. ................................................ 148! Figure 6.2. Influence of geography on virome composition. 72 virome data sets were compared with each other using the Bray !Curtis similarity matrix based on relative abundance of viral families. A, Principal Coordinates Analysis (PCoA) plot presenting the difference in the virome composition. Convex hulls were used to group observations by ocean. Closed and open symbols repres ent ballast and harbor waters, respectively. B, Analysis of similarity (ANOSIM) result to identify the difference in the virome composition. Bold text indicates a significant difference between ocean viromes. ....... 156! xiv Figure 6.3. Response of the top three viral families contributing most to the differences between oceans to geographical variation. Relationship between relative abundances of Microviridae , Podoviridae , and Myoviridae and samplesÕ geographic origin was examined. Latitude and longitude are expressed in decimal scale. R was the Pearson correlation coefficient for the relative abundance of viral families against the either latitude or longitude in 72 data set s. Bold text indicates a statistical significance. Green and red dots represent vessels with ballast waters arriving in the Port of Los Angeles/Long Beach and the Port of Singapore, respectively. ....................................... 163! Figure 6.4. Comparison of virus richness between ballast and harbor waters. Virus richness was defined as a total number of identified viral families. A, Boxplot presenting virus richness of individual sample. B, Boxplot presenting virus richness of ballast and harbor water groups. Bonferroni !corrected pairwise t!tests were conducted to test for significant differences in virus richness between groups. Black lines within boxplots represent median values and whiskers ind icate minimum and maximum values. CABW, ballast water from the Port of Los Angeles/Long Beach (LA/LB); CAHW, harbor water from the Port of LA/LB; SGBW, ballast water from the Port of Singapore; SGHW, harbor water from the Port of Singapore. ....................................................................... 167! Figure 6.6. Global distribution of eukaryotic viral pathogens. Samples containing viral pathogen !associated contigs were represented in the map. B, ballast water; H, harbor water; D, where viral pathogen !induced disease was found. ......................................... 175! !!J!!!!!!!!!!!!!!!!!!!!!5).1("*'8' ''$%(*+!35($+%'' !!H8989'-:;:<=>?:;<'@AB;CDA'E>FF>?@'G>@HB' a(+=>!=:6%@%6%'&!&(:;!=&!=&B8A6=6%8>O!=>7! 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U"Z!(&%>&6A(+'>6!=>7!6;'!R%<;6[ #:)'A!f]I!GA85'!9=&6'A!+%PM! ,55A'@%=6%8>j!GT?O!B)=D('FC8A+%>%6M! 57 Figure 4.3 (cont Õd) !!K]P9I9I9I9'2:B>F'O:L'H^@B>O@:;<'><@:@> @:=H'15*'LH@HO@:;<' ,C6'A!DG[1!&6=>7=A7!:(A@'!<'>'A=6%8>O!6L8!&'6&!8C!& 6'A%)'!B;8&B;=6'!5(CC'A'7! &=)%>'!UG"/O!fMV!+9!4= HaG3 fO!JMf!+9!*a HaG3 fO!JVe!+9!4=[)O!=>7!HMe!+9!*[)!%>! >=>8B(A'!L=6'AO!Ba!eMHZ!L'A'!&''7'7!L%6;!B;=<'&!9/H !=>7!G;%Jef!=6!6L8!7%CC'A'>6! )'@')&O!JI K!=>7!JI X!GT?&!B'A!+R!8C!G"/M!2;'!&6=A6%>7! 14,!'P6A=:6%8>!L'A'!%>:A'=&'7!CA8+!6;'!A':8++'>7'7! &6=A6%>6&!>''7'7!C8A!6;'!'P6A=:6%8>!L'A'!% >:A'=&'7!BA8B8A6%8>=))#!L%6;! %>:A'=&'7!&6=A6%>7!G;%Jef!L'A'! (&'7!C8A!@%A=)!>(:)'%:!=:%7!'P6A=:6%8>!L%6;!b.,=+B! 9%>0)(6'!Q%A(&!/B%>!*%6O!b.,=+B! ?)6A=/'>&!Q%A(&!*%6O!=>7!14'=&#!G)(&!9%>%!*%6O!L;%) '!KXI!nR!8C!&''7'7!G"/!L=&!(&'7! L%6;!b.,=+B!Q%A=)!14,!9%>%!*%6!Ub%=<'>O!Q=)'>:%=O![ ,O!?/,ZM!JOIII!nR!8C!&''7'7! 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'P9I9I9P9'5;KN>B:?;<';J'=:B>F'O:L'H^@B>O@:; <'KH@A;L?' .>!8A7'A!68!:8+B=A'!6;'!=5%)%6#!8C!:8++'A:%=)!S%6&! 68!'P6A=:6!586;!@%A=)!-4,!=>7! 14,!=>7!68!;=>7)'!%>:A'=&'7!&6=A6%>&!L'A'!&''7'7!L%6;! S>8L>!:8>:'>6A=6%8>&!8C!B;=<'&!9/H!=>7!G;%Jef!=>7! '@=)(=6'7!5#!DG[1M!T8A!586;! B;=<'&!9/H!=>7!G;%Jef!=6!586;!&''7%>:'>6A=6%8 >&!8C!JI K!=>7!JI X!GT?&!B'A!+RO! 6;'!(&'!8C!b.,=+B!9%>0)(6'!Q%A(&!/B%>!*%6!#%')7'7!6 ;'!)8L'&6![ 2!@=)('&!C8A!DG[1!L%6;! &%<>%C%:=>6!7%CC'A'>:'!=+8>0)(6'!Q%A(&!/B%>!*%6!L=&!5'&6!&(%6'7!C8A! &%+()6=>'8(&)#!'P6A=:6%>7!14,!5':=(&'![ 2!)'@')&!=A'!%>@'A&')#!BA8B8A6%8>=)!68!6;'!=+8(>6!8C !6=A<'6! >(:)'%:!=:%7!%>!=!&=+B)'M!3>!6;'!86;'A!;=>7O!6;'!(& '!8C!14'=&#!G)(&!9%>%!*%6!#%')7'7!6;'! ;%<;'&6![ 2!@=)('&!C8A!586;!B;=<'&!9/H!=>7!G;%Jef!=6!586;!&'' 7%>:'>6A=6%8>&O! &(<<'&6%>:#!%>!A':8@'A%> (:)'%:!=:%7&M![ 2!@=)('&!<'>'A=6'7!CA8+! 6;'!(&'!8C!b.,=+B!Q%A=)!14,!9%>%!*%6!L'A'!=)&8!%>:) (7'7!%>!6;'!'CC%:%'>:#!:8+B=A%&8>M! a8L'@'AO!%6!&;8()7!5'!>86'7!6;=6!)8L'A!&6=A6%>(:)'%:!=:%7&!L%6;!b.,=+B!Q%A=)!14 ,!9%>%!*%6M!! "=&'7!8>!6;'!)8L'&6![ 2!@=)('!=+8>0)(6 '!Q%A(&!/B%>!*%6!L=&!(&'7!C8A!&%+()6=>'8(&)#!'P6A=:6% >7!14,!C8A!6;%&! A'&'=A:;M! 60 Figure 4 .4. Comparison of qPCR CT value for viral nucleic acid ex tracts from seeded water with 10 5 and 10 6 PFUs/mL of MS2 (A) and PhiX174 (B). The error bars represent !"#$%#$"#&%#&"#!'%%()%"# !'%%()%*# !"#$%&#'( )'*+,' !'+#,#-#.#+#,#-#-#!"#$%&'($ !")$%&'($ !"#$%#$"#&%#!'%%()%"# !'%%()%*# !"#$%&#'( )'*+,-./0' 1'+#,#-#.#+#,#-#.#!"#$%&'($ !")$%&'($ 61 Figure 4.4 (cont Õd) standard deviation of the C T value calculated from six replicates. Different letters in the figure indicate significant differences according to Bonferroni LSD multiple comparison tests (p < 0.05). Abbreviation s: qPCR, quantitativ e PCR; CT, cycle threshold; PFUs, plaque Ðforming units ; LSD; least significant difference . !!XHP9M9'!H?OB:N@:;<';J'K>@HB:>F?'>B:<>FX]:'A=))#O!=!@%A=)!+'6=<'>8+%:!&6(7#!%&!:8+B8&'7!8C !6;A''!+=%>!&6'B&j!UJZ!@%A8+'! BA'B=A=6%8>O!UHZ!;%<;F6;A8(<;B(6!&'D('>:%>7!UV Z!5%8%>C8A+=6%:&!=>=)#&'&M!,!B%B')%>'! 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T%<(A'!KMH[ZM!! !!hV!#:DCBH'T9I9 !2=P8>8+%:!BA8C%)'!8C!6;'!5=))=&6!=>7!;=A58A!L=6'A! @%A8+'&M!1')=6%@'!=5(>7=>:'!8C!:8>6%<&!L'%<;6'7!5#! &'D('>:'!A'=7&! 5=&'7!8>!6=P8>8+%:!=&&%<>+'>6!8C!:8>6%<&!U,ZM![8>6% <&!6;=6!L'A'!=&&%<>'7!68!@%A=)!6=P=!5(6!7%7!>86!+'' 6!6;'!&')':6'7!90E,4! .'!"!!!!!! #$%&'( !""!#)*+,%&-( !".!#/01'%&-%( !2"!!!#.0%-*( !2.!#/01'%&-%( !3"!#3&45&6,*( !3.!#/01'%&-%( !7"!#)*+,%&-( !!88&6*'9 !:;<= !>>:@@<; !><> !; !;;;F !!",% ("!!!!%51$4%$/" !!!!)-!!!!/)$ 6'!!!!7"*68#"4 !!!!59!!!!&"%4' !!!! 94 Figure 5 .2 (cont Õd) parameters were placed under ÒNot assigned,Ó and contigs that did not have any hits to known sequences in t he databases were placed under ÒNo hits.Ó Types of viral genomes (B), types of virus hosts (C), and contigs assigned to viral families (D) in the ball ast and harbor water viromes. Viral families whose maximum relative abundances across eight viromes less t han 3% were represented as ÒOthers aÓ. 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HKOhJf! hV]!]MH!!!!!""!HXe!XVX!IMJ!""!HXh!XHJ!IMJ!!!!! "a! VVOfVJ! eIV!JIMK! "a! VVOVf]! ehh!JIMK! !!!!."!]OKKh!eKV!HMe!."!]OKIK!eXh!HMe!!!!! .a! VIOhII! JOJeh! hM]!.a! VIOKXV! hff!hMe!!!!!9"!JIOhIH!]IH!VMK!9"!JIO]fJ!]eK!VMf!!!!! 9a! KO]hV! hf]!JM]!9a! XOIVV! ]hV!JMh!!!!!G"!ehOIVI!hJe!HKMH!G"!e]OJ]h!JOIIH!HfMh!!!!! =!4(+5'A!8C!=)%<>'7!A'=7&!68!=!A'C'A'>:'!<'>8+'!&'D( '>:'M! 111 Table 5.8 (cont Õd) b Number of bases of a reference genome sequence aligned by reads. Bold letters indicated complete genome sequences of Koi herpesvirus retrieved from the NCBI RefSeq database. !!JJHT9M9T9'5;KN>B:?;<'>K;@',>cH?'E>FF>?@'>BE;B'G>@HB'=:B;KH?' [8+B=A%&8>&!8C!@%A8+'&!8C!5=))=&6!L=6'A&!CA8+!R=S'& !0A%'O!a(A8>O!9%:;%<=>O!=>7! 3>6=A%8!=>7!;=A58A!L=6'A&!CA8+!R=S'!/(B'A%8A!L'A'!: 8>7(:6'7!68!'P=+%>'!6;'!&%+%)=A%6%'&! 5'6L''>!)=S'&!=>7!68!%>&B':6!L;'6;'A!6;'!;=A58A!L=6 'A&!>'=A!@'&&')&!L'A'!A'C)':6%@'!8C!6;'! A'&B':6%@'!5=))=&6!L=6'A&M!T8A!@%A8+'!:8+B=A%&8>O!= >>86=6%8>t%>7'B'>7'>6!=BBA8=:;'&! 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K7O4 K7O. 7O. 7O4 K7O4 K7O. 7O. 7O4 7OP .'G--%9&*,+' !>!#@:F( !G--%9&*,+' !:!#>@!!!!!!!!1&)$= !!!!;;!!!!!!!!EFH'T9V9 !/%+%)=A%6#!+=6A%P!8C!:8>6%<&!5'6L''>!5=))=&6!=>7!; =A58A!L=6'A!@%A8+'&!(&%>6=A%8Z !-)' U/(B'A%8AZ !$-' Ua(A8>Z !$)' U/(B'A%8AZ !6-' U9%:;%<=>Z !6)' U/(B'A%8AZ !1-' U3>6=A%8Z !,>cH'-;CBDH@ ',>cH'1>=:< '.-' U0A%'Z 'KJMHVJ!XXMHhH!KXM]XJ!KVMfIK!VKMVVe!XXMIIf!XJMeXH!VK MIII!VIM]JI! --' U3>6=A%8Z '!KIMK]H!XhMhXf!V]MI]h!XVMHIe!fJMIfI!eIMX]f!KeMIXe!K IMJ]h! -)' U/(B'A%8AZ '!!KHM]Xe!KIMfe]!VVMhfh!XVMVXV!KeMJKJ!VJMJVh!HeMHV]! $-' Ua(A8>Z '!!!fJM]eK!KVMhIf!fKMKHh!eXMVVI!feMeJJ!fJMIKf! $)' U/(B'A%8AZ '!!!!VHMeIK!KVMIIK!f]MJIV!HfM]hX!HJMJIH! 6-' U9%:;%<=>Z '!!!!!HeMJJV!K]MVIJ!KJMVhh!fKMXV]! 6)' U/(B'A%8AZ '!!!!!!KIMheX!HXMJhf!HHMhHe! 1-' U3>6=A%8Z '!!!!!!!XVMVeh!K]MIXX! ,>cH'-;CBDH@' !!!!!!!!eeMXeI! ,>cH'1>=:<' !!!!!!!!!R=S'!"8(A<'6!=>7!R=S'!G=@%>!@%A8+'&!CA8+!6L8!6'+B'A =6'!CA'&;L=6'A!)=S'&!%>!TA=>:'!L'A'!%>:)(7'7!=&!=>! 8(6)%'A!EFH'T98Q9 !/%+%)=A%6#!+=6A%P!8C!:8>6%<&!5'6L''>!5=))=&6!=>7!; =A58A!L=6'A!@%A8+'&!(&%>6=A%8Z !-)' U/(B'A%8AZ !$-' Ua(A8>Z !$)' U/(B'A%8AZ !6-' U9%:;%<=>Z !6)' U/(B'A%8AZ !1-' U3>6=A%8Z !,>cH'-;CBDH@ ',>cH'1>=:< '.-' U0A%'Z 'XMIJV!fMhHX!VMKfe!HMhHI!VM]hK!VMeKf!JMX]e!IMVfH!IMH Xe! --' U3>6=A%8Z '!hMVhV!XMfX]!VM]HX!JIM]XJ!eMHJX!JJMHXf!HMJh]!IMfVK! -)' U/(B'A%8AZ '!!HMXKf!fMJfH!VMHef!KMeKJ!JMHHe!IMHKH!IMHfI! $-' Ua(A8>Z '!!!JMK]X!VMVJh!HMIhK!XMhKK!IMK]K!IMHJK! $)' U/(B'A%8AZ '!!!!HMIKH!VMVHJ!IMeJJ!IMJVf!IMJVI! 6-' U9%:;%<=>Z '!!!!!VMJeK!eMeKH!JMV]]!IMVHJ! 6)' U/(B'A%8AZ '!!!!!!IMhV]!IMHKH!IMJ]f! 1-' U3>6=A%8Z '!!!!!!!HMhJh!JM]hJ! ,>cH'-;CBDH@' !!!!!!!!HMJXJ! ,>cH'1>=:<' !!!!!!!!!R=S'!"8(A<'6!=>7!R=S'!G=@%>!@%A8+'&!CA8+!6L8!6'+B'A =6'!CA'&;L=6'A!)=S'&!%>!TA=>:'!L'A'!%>:)(7'7!=&!=>! 8(6)%'A!B:?;<';J'@AH'&BH>@',>cH?'E>FF>?@'> BE;B'G>@HB'=:B;KH?'G:@A';@AHB' >WC>@:O'=:B;KH?' 2;'!EA'=6!R=S'&!5=))=&6!=>7!;=A58A!L=6'A!@%A8+'&!L' A'!=)&8!:8+B=A'7!68! BA'@%8(&)#!B(5)%&;'7!@%A8+'&!%>!CA'&;L=6'A!=>7!+=A% >'!L=6'AM!2;'!;%'A=A:;%:=)!:)(&6'A%>=)#&%&!A'@'=)'7!6;=6!=D(=6%:!@%A8+'&!:8()7!5 '!:)=&&%C%'7!%>68!6L8!A'BA'&'>6=6%@'! 7!+=A%>'!L=6'A!@%A8+'!U T%<(A'!KMfZO!;%<;)%<;6%>6!'>@%A8>+'>6&!:8>6=%>!(>%D('!@%A8+'!&%<>=6 (A'&M!,+8>7!;=A58A!L=6'A!@%A8+'&!L' A'!:)8&')#!A')=6'7!68!'=:;!86;'A!=>7! :)(&6'A'7!L%6;!6L8!@%A8+'&!CA8+!6;'!8)%<8+'&86A8B;% :!R=S'!G=@%>!=>7!6;'!+'&86A8B;%:! R=S'!"8(A<'6!%>!TA=>:'M!Q%A8+'&!CA8+!7'&'A6!B8>7&!= >7!=>!=D(=:()6(A'!B8>7!<'>'A=6'7!=! &(5!,>6=A:6%:!)=S'!=>7!A':)=%+'7! =>7!B86=5)'!L=6'A!L'A'!=<7%@%7(=))#!=>7! 7%&6=>6!CA8+!6;'!86;'A!CA'&;L=6'A! @%A8+'&M!! 118 Figure 5.4. Comparison of the ballast and harbor water viromes with published freshwater viromes based on sequence similarity with a cross -TBLASTX search. The six viromes (AB, BH, IB, IH, MH, and PB) from this research are highlighted in blue. TBLASTX Ð2008OMZst3viral200m 2008OMZst5viral200m 2008OMZst3viral10m 2008OMZst5viral55m 2008OMZst5viral90m 2008OMZst3viral90m British_Columbia___96_2004 Gulf_of_Mexico___96_01 Arctic_Vir___2002Coral_Atoll_Kiritimati Coral_Atoll_Palmyra Coral_Atoll_Tabueran Sargasso_Sea___2005Coral_Atoll_Kingman Tampa_Bay_induced GS122GS117GS112GS108RW_Park_DNA RW_Effluent_DNA RW_Nursery_DNA Potable_DNA RW_Effluent_RNA RW_Nursery_RNA Antarctic_Lake_Spring Antarctic_Lake_Summer Lake_Pavin Lake_Bourget IB_fa PB_fa IH_fa MH_fa AB_fa BH_fa ElBerbera IlijMolomharTilapia_Channel___0806Tilapia_Channel___1105Tilapia_Channel___0406Prebead_pond___0406!0.50.00.51.0distance ! hclust("average") Type of virome Freshwater Private Seawater !!!!!! !"#$#%&'()*&'+,+- !"#$%!&'$()*$( +,-./012034536 7!./0%(/%'12%**#0'+,+- !"#$%!&'$()*$( +,-./012034536 7!./0%(/%'12%**#0'33+4 !"#$%!&'$()*$( +,-./012034536 7!./0%(/%'12%**#0'+5+- !"#$%!&'$()*$( +,-./012034536 7!6)0)72%" !"'898-8()*$( +,-./012034536 7!80/9!"'898-8()*$( +,-./012034536 7!:0;#"$#"% !"'898-8()*$( +,-./012034536 7!;?*$( @AA2B538 7!=;!":-08;!<8=0/%!&'$()*$>?*$( @AA2B538 7!8?*$( @AA2B538 7!!;!":-08;!<8=0/%!&'$()*$>?*$( @AA2B538 7!8;!":-08;!<8=0/%!&'$()*$>?*$( @AA2B538 7!6?*$( @AA2B538 7!>%?#';)@"A#B !"C-8340()*$( +,-./012034536 7!>%?#'!%C/* !"C-8340()*$( +,-./012034536 7!=*B%"DED'>%?#'F@77#" !"$3;8-4D4()*$( +,-./012034536 7!=*B%"DED'>%?#'F("/*A !"$3;8-4D4()*$( +,-./012034536 7!GH'I@"J#"K'GI= !"C<%!&'$(?*$( +,-./012034536 7!GH':L@#*B'GI= !"C<%!&'$(?*$( +,-./012034536 7!!)B%$0#'MI= !"C<%!&'$()*$( +,-./012034536 7!GH'I@"J#"K'MI= !"C<%!&'$()*$( +,-./012034536 7!GH':L@#*B'MI= !"C<%!&'$()*$( +,-./012034536 7!GH'!%"?'MI= !"C<%!&'$()*$( +,-./012034536 7!NF3+5 !"@3E583!F4083()*$( +,-./012034536 7!NF33O !"@3E583!F4083()*$( +,-./012034536 7!NF33P !"@3E583!F4083()*$( +,-./012034536 7!NF3OO !"@3E583!F4083()*$( +,-./012034536 7!.%7(%';%K'/*&@D#& !"C<%!&'$()*$( +,-./012034536 7!1)"%0'=B)00'Q/*A7%* !"<530!@/A83E%!+845G4!F4083()*$( +,-./012034536 7!F%"A%JJ)'F#%'O++4 !"'8-68//.!'08()*$( +,-./012034536 7!1)"%0'=B)00'.%$@#"%* !"<530!@/A83E%!+845G4!F4083()*$( +,-./012034536 7!1)"%0'=B)00'!%07K"% !"<530!@/A83E%!+845G4!F4083()*$( +,-./012034536 7!1)"%0'=B)00'Q/"/E7%E !"<530!@/A83E%!+845G4!F4083()*$( +,-./012034536 7!="DED'R/"'O++O !"$-4D4!F4083()*$( +,-./012034536 7!N@0S')S'6#T/D)'U-'+3 !":2AH!.H!I0J54.()*$( +,-./012034536 7!;"/EJ2'1)0@7*/%'U-'O++, !"K-5D/9!#.A2BL58()*$( +,-./012034536 7!O++5V6WJBXC/"%0U+7 !"#95A0()*$( +,-./012034536 7!O++5V6WJB4C/"%0U+7 !"#95A0()*$( +,-./012034536 7!O++5V6WJB4C/"%0447 !"#95A0()*$( +,-./012034536 7!O++5V6WJBXC/"%03+7 !"#95A0()*$( +,-./012034536 7!O++5V6WJB4C/"%0O++7 !"#95A0()*$( +,-./012034536 7!O++5V6WJBXC/"%0O++7 !"#95A0()*$( +,-./012034536 7!=Y@%D@0B@"#Z()*&Z M#J#"BZ()*&Z .#7(#"%B#Z0%?#Z =*B%"DEDZ0%?#Z G#D0%/7#&Z%*&Z()B%$0#Z[%B#"Z !"#$%&'(#") *'"+,#)&'(#") 119 Figure 5 .4 (cont Õd) based comparison was not available for the other two viromes (BB and MB), due to insufficient numbers of input contigs. Virom e names were retrieved from the MetaVir. Sam pling site, virome fraction, and sequencing platform of each virome were shown in the parentheses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g!?M/M!0G,ZM!! 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C8A!'=:;!&=+B)'O!L;%:;!:8>6=%>'7! :8>:'>6A=6'7!=>7!B(A%C%'7!@%A=)!B=A6%:)'&M!2;'!A'&( )6%>7!;=A58A!L=6'A!@%A8+'! 7=6=!&'6&!:8+BA%&'7!VM]!5%))%8>!JIIN5=&'!B=%A!U5BZ! B=%A'7N'>7!.))(+%>=!A'=7&!L%6;!=>! =@'A=<'!8C!KHMH! W!VIMh !U+'=>!W!&M7MZ! +%))%8>!A'=7&!U2=5)'!XMVZM!2;'!@%A8+'!7=6=!&'6&! :=B6(A'7!<'>8+'&!8C!586;!-4,!=>7!14,!@%A(&'&!BA'&'> 6!%>!5=))=&6!=>7!;=A58A!L=6'A&M!! 148 Figure 6.1. Relative distribution of viromes from ballast and harbor waters. Pie chart s represent a mean relative abundance of assigned viral families (three replicates from 24 samples) . ÔOthersÕ are v iral families whose maximum relative abundances across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igure 6 .1 (cont Õd) viromes are less than 3% (including RNA viruses) . Vessels with ballast waters arriving in the Port of L os Angeles/Long Beach are shown as a green star and the Port of Singapore as a red star. Circles and squares in the map indicate ballast waters exchanged beyond and wit hin 200 nautical miles from nearest shoreline, respectively. Abbreviations: ds, double !stranded; ss, single !stranded. !!JKI(>EFH'U9M9 !3@'A@%'L!8C!6;'!&'D('>:'!A'=7&!=>7!6;'!=&&'+5)'7!: 8>6%<&!8C!6;'!@%A8+'!)%5A=A%'&! /=+B)'!⁄!1=L!A'=7&! ⁄!2A%++'7! A'=7&! ⁄![8>6%<&! 9'=>!:8>6%<6;!U5BZ! 9=P!:8>6%<6;!U5BZ! 9%>!:8>6%<6;!U5BZ! 9=BB%>'7! Y!1'=7&! =&&%<>'7! [,-3J! JfOXIeOfVH!JVOVI]OHXI!JhOKJV!Xe]!H]OHff!HII!]IMV]!KOVJX!HeMHI![,-3H!feOfheO]J] !fKO]IVOJ]e!XVOh]e!eII!VVOH]I!HII!]hMIX!JeO]Kf!HeMhI![,-3V! VeOKeIOeJI!VXOVVVOfKX!XVOheK!eHV!HJOe]f!HII!hJMf]!J]Of]I!H]MhI![,/[J!VeOKKJOXhI !VXOJXIOXXJ!XJOVhI!ehK!HfOXhV!HII!hKMI]!JhOVXJ!VJMKI![,/[H! V]OHKVOHVH!VXOh]KOeH]!K]OJ]]!eKh!HJOHVH!HII!hfMV]!J]OI]H!VJMJI![,/[V!VeOKVVOHHI !VXOHheOJ]J!XVOhIe!eXh!J]O]VK!HII!hVMhJ!JhOh]]!VJMVI![,2RJ! VfOVKhOHIX!VVOVVKOhhJ!JHOXeH!]HV!JIOeVJ!HII!hJMff!fOHeI!VVMeI![,2RH!VJOe]fOffX !VIOeIHO]hf!HJOHJf!]Jf!JhOI]I!HII!hIM]K!XOhe]!VHMhI![,2RV! VKOVJHOVHI!VVOh]hOVKe!JHOHXV!]Je!JJOf]J!HII!]VMff!fOIVh!VHMhI![",RJ!VeOHIhOHH] !VKOeHXOeII!JfXOVhK!eIK!KIOJfJ!HII!e]M]I!ffOKVK!VIMfI![",RH! VKOeKXOJe]!VfOH]XOJhe!JKXOHHK!XhH!KKOIff!HII!e]MIK!fKOhX]!HhMfI![",RV!VVOHeHOVVH !VJOhXIOIhI!JKeOKhf!eIV!eJOHhJ!HII!e]MeJ!feOJef!HhMhI![[,1J! HhOKX]OhXX!H]OJfXOJVf!e]OJI]!efH!hJOKIX!HII!]IMJ]!HHOVe]!H]MeI![[,1H!HhOfehOKXH !H]OHXJOeIh!]IOhJh!efK!XXOeJK!HII!]JMXK!HVOKKf!HhMJI![[,1V! VJOVHeOhIX!VIOH]HOehJ!]VO]H]!eff!eKOfJe!HIJ!]JMee!HfOVeV!HhMJI![[0"J!HVOHf]O]XH !HHOK]eOIeX!XKOKhJ!XV]!fhOf]f!HII!]KMVH!JhOeJ]!VIMJI![[0"H! HfOJfIOhIH!HVOVXhOJfJ!KfOhK]!XVf!eIOJHh!HII!]KMHh!JKOXHe!H]MfI![[0"V!HfOhKHOHJI !HfOHJHO]VK!XHOJKK!XVf!f]OIKK!HII!]KMKH!JeOh]H!H]MhI![[3/J! H]OIKHOfHX!HeOHXIOfKh!JJKOfXJ!XHI!VKOIJK!HII!eIMVJ!VIOJeJ!HXMJI!!!JKJ(>EFH'U9M !U:8>6i7Z! /=+B)'!⁄!1=L!A'=7&! ⁄!2A%++'7! A'=7&! ⁄![8>6%<&! 9'=>!:8>6%<6;!U5BZ! 9=P!:8>6%<6;!U5BZ! 9%>!:8>6%<6;!U5BZ! 9=BB%>'7! Y!1'=7&! =&&%<>'7! [[3/H! 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G=:%C%:!3:'=>!CA8+!6;'!86;'A!:)(&6'A&!UT%<(A'!XMH"Z M!2;%&!C(A6;'A!&(<<'&6'7!6;=6!+=A%>'! @%A8+'&!=A'!>86!&6A(:6(A'7!8>)#!5#!<'8&!5(6!=)&8!5#!)8:=)!'>@%A8>+'>6=)! !!JKK:8>7%6%8>&!=&!A'B8A6'7!5#!=!A':'>6!&6(7# !U"A(+!'6!=)MO!HIJKZM!G=%AL%&'!:8+B=A%&8>&! &;8L'7!6;=6!@%A8+'&!8C!'=&6'A>!G=:%C%:!3:'=>!=)8>7%=>!3:'=>!U1!l!IM XhJO! 7!o!IMIIJZ!8A!L'&6'A>!G=:%C%:! 3:'=>!58A7'A%>!,&%=!U1!l!IMHe]O! 7!o!IMIIJZO!L;%)'!6;%&!&'B=A=6%8>!L=&!>86! 85&'A@'7!L%6;!6;8&'!8C!8B'>!G=:%C%:!3:'=>M! 156 Figure 6.2. Influence of geography on virome composition. 72 virome data sets were compared with each other using the Bray !Curtis similarity matrix based on relative abundance of viral families. A, Principal Coordinates Analysis (PCoA) plot presenting the d ifference in the virome composition . Convex hulls were used to group observations by ocean. Closed and open symbols represent ballast and harbor waters, respectively. 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J%-(@+%c'9'&'4(%) IMIIIIJ!IMIIIIV!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIV! D'+%9'&3") IMIIIIJ!IMIIIIV!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIV! J3/0(9'&'4(%) IMIIIIJ!IMIIIIV!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIV! 8(+(#*$%&7%"9'&'4(%) IMIIIIJ!IMIIIIH!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIH! !/4*&/(9'&'4(%) IMIIIIJ!IMIIIIH!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIH! :$(64*9'&'4(%) IMIIIIJ!IMIIIIH!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIH! Q3&&'9'&'4(%) IMIIIII!IMIIIIJ!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIJ! ,%9'9'&'4(%) IMIIIII!IMIIIIJ!JIIMIIIII!IMIIIII!IMIIIII!IMIIIII!IMIIIIJ! !!JXV'#:DCBH'U9M9 !1'&B8>&'!8C!6;'!68B!6;A''!@%A=)!C=+%)%'&!:8>6A%5(6 %>:'&! 5'6L''>!8:'=>&!68!<'8M!1')=6%8>& ;%B!5'6L''>!A')=6%@'!=5(>7=>:'&!8C! 8'#&*9'&'4(% O!2*4*9'&'4(% O!=>7! 80*9'&'4(% !=>7!&=+B)'&i!<'8!L=&! 164 Figure 6 .3 (cont Õd) examined. Latitude and longitude are expressed in decimal scale. R was the Pearson correlation coefficient for the relative abundance of viral families against the either latitude or longitude in 72 data sets . Bold text indicates a statistical sign ificance . Green and red dots represent vessels with ballast waters arriving in the Port of Los Angeles/Long Beach and the P ort of Singapore, respectively. !!JXKU9M9I9'"JJHO@';J'H<>DHKH<@R'>F'=>B:>EFH?';<'@AH';OH><' =:B;KH' "=))=&6!L=6'A!'P:;=><'!8B'A=6%8>!;=&!5''>!:8>&%7'A' 7!68!5'!'CC%:%'>6!68!BA'@'>6! 6;'!%>6A87(:6%8>!8C!>8>N%>7%<'>8(&!&B':%'&!5=&'7!8> !BA'@%8(&!C%>7%><&!L;'A'!)8L'A!@%A=)! =5(>7=>:'&!U)8L!>(+5'A!8C!@%A=)!B=A6%:)'&Z!L'A'!C8( >7!%>!6;'!+%7N8:'=>!A')=6%@'!68! :8=&6=)!'>@%A8>+'>6&!U[8:;)=>!'6!=)MO!JhhVg!"8';+'! '6!=)MO!JhhVg![())'#!=>7! `')&:;+'#'AO!HIIHZM!-('!68!)%+%6'7!':8)8<%:=)!BA86' :6%8>!=CC8A7'7!5#!5=))=&6!L=6'A! 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L=6'A!'P:;=><'!%>!A'7(:%>(+5'A!8C!7%CC'A'>6! @%A(&'&!L=&!'@=)(=6'7!5#!:8+B=A%>'&&!5'6L''>!5=))=&6!=>7!;=A58A!L=6'A&M!a 'A'O!@%A(&!A%:;>'&&!L=&!7'C%>'7!=&!=! 686=)!>(+5'A!8C!%7'>6%C%'7!@%A=)!C=+%)%'&!%>!6;'!7= 6=!&'6&M!3@'A=))O!@%A(&!A%:;>'&&!@=A%'7! :8>&%7'A=5)#!=:A8&&!&=+B)'&!UA=><'7!CA8+!HI!68!KXg! T%<(A'!XMf,ZM!2;'!5=))=&6!=>7!;=A58A! L=6'A&!:8))':6'7!CA8+!6;'!G8A6!8C!/%><=B8A'!UfJMf! W!XMX Z!;=7!&%<>%C%:=>6)#!;%<;'A!@%A(&! A%:;>'&&!6;=>!6;8&'!CA8+!6;'!G8A6!8C!R,\R"!UH]MK! W!fMJ O!7!o!IMIIIJg!T%<(A'!XMf"ZM!`;'>! !!JXX:8+B=A%>'&&!5'6L''>!5=))=&6!=>7!;=A58A !L=6'A&!=6!'=:;!B8A6O!;=A58A!L=6'A&! UffMJ! W!eMeZ!;=7!&%<>%C%:=>6)#!;%<;'A!@%A(&!A%:;>'&&!6;=>!5 =))=&6!L=6'A&!UV]Me! W!VMh Z!%>!6;'! G8A6!8C!/%><=B8A'!U 7!o!IMIKZO!L;%)'!>8!&%<>%C%:=>6!7%CC'A'>:'!L=&!85&'A @'7!%>!6;'!G8A6!8C! R,\R"M! !!JXe!#:DCBH'U9P9 ![8+B=A%&8>!8C!@%A(&!A%:;>'&&!5'6L''>!5=))=&6!=>7!; =A58A!L=6'A&M!Q%A(&! 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d8A!A8)'!%>!7'6'A+%>%> 7=>:'!8A!A%:;>'&&!8C!@%A(&'&!BA'&'>6!%>! !!JeI5=))=&6!L=6'AM! 171 Figure 6.5. Effect of engineered, management, and environmental variables on the differences in the ocean virome. Response of virus richness to engineered, management, and environmental variables was examined. A, Relationship between virus richness and engineered and management variables. B, Relationship between virus richness and environmental variables. R was the Pearson correlation coefficient for the virus richness against the variables . Bold text indicates a statistical significance . Green and red dots represent ballast and harbor waters collected from the Port of Los Angeles/Long Beach and the Port of Singapore, respectively . !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!02040608010001020304050Time in ballast tanks (day) Virus richness !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!02040608001020304050Distance from the nearest shoreline (nautical mile)Virus richness !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!0200400600800100001020304050Distance from the nearest shoreline (nautical mile)Virus richness !!!!!!!! !"#"$%&%#'()"*+",-%(((((((((( !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!0200400600800100001020304050Distance from the nearest shoreline (nautical mile)Virus richness .(/(0(12345( !(6(121117(( "!#!$!%&'()! !!#!%&*'+!! "!#!$!%&*),! !!#!%&')*!! "!#!$!%&*))! !!#!%&*-(! !!!!!!!! 8#$+#%%*%9()"*+",-%(((((((((( :(( 172 Figure 6 .5 (cont Õd) !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!0102030405001020304050LatitudeVirus richness !"#"$"%&'()" !"*"%&%%%+"" !!!!!!!! ,-./01-23-456".50/57638" !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!152025303501020304050SalinityVirus richness !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!010203040500246810LatitudeVirus richness (phage) !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!0102030405005101520LatitudeVirus richness (vertebrate virus) !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!0102030405005101520LatitudeVirus richness (invertebrate virus) !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!0102030405005101520LatitudeVirus richness (plant virus) !"#"$"%&9:(" !"*"%&%;"" !"#"$"%&(()" !"*"%&%+"" !"#"$"%&);+" !"*"%&%%%+"" !"#"$"%&')(" !"*"%&%%%+"" !"#"$"%&):;" !"*"%&%%%+"" !"#$%& '%()%*(#)%&+,(-.& /0+%()%*(#)%&+,(-.& !1#0)&+,(-.& <"" !!Je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i! <'8!L=&!(&'7!=&!A'BA'&'>6=6%@'!8C!8A% <%>=)!L=6'A!6'+B'A=6(A'!5=&'7!8>!6;'%A! &%<>%C%:=>6!A')=6%8>&;%B!U1!l!N!IMeffO! 7!o!IMIIIJO!7=6=!>86!&;8L>ZM!,!:8AA')=6%8>!=>=)#&%&! A'@'=)'7!6;=6!@%A(&'&!L'A'!BA'&'>6!%>!;%<;'A!A%:;>' &&!>'=A!6;'!'D(=68A!=>7!)8L'A!A%:;>'&&! =6!;%<;'A!)=6%6(7'&M!T(A6;'A+8A'O!'=:;!;8&6!6!7'&;%B!L%6;!6'+B'A=6(A'O !=>7!6;'!L'=S'&6!A')=6%8>&;%B!L=&! C8(>7!%>!B;=<'!6)#O!6;%&!A'&()6!&(<< '&6'7!A'&6A%:6'7!<'8!8C!86;'A!'(S=A#86%:!U%>:)(7%>%+=)! =>7!B)=>6Z!@%A=)!&!A'<=A7%>@=&%8>!8C!)8:=)!5%8)8<%:=) !&#&6'+&!U(>)%S'!6;'!;8+8<'>'8(&! 7%&6A%5(6%8>!8C!B;=<'&!=:A8&&!6;'!8:'=>&ZM! !U9M9M9'1;@H<@:>F':<=>?:;<'EX'B>BH'=:B>F'N>@A;DH!=!&%<>%C%:=>6!%>:A'=&'!%>!<)85=)!&;%B!6A=CC%: !=>7!%6&!:8>6%>(8(&! +8@'+'>6!8C!5=))=&6!L=6'AO!6;'!B86'>6%=)!C8A!@%A=)! B=6;8<'>&!BA'&'>6!%>!5=))=&6!=>7!;=A58A! L=6'A&!L=&!'P=+%>'7!68!=77A'&&!6;'!;8&6!B8B()=6%8>& !=6!A%&S!8C!%>C':6%8>M!.>!6;%&!A'&'=A:;O! =!>(+5'A!8C!:8>6%<&!L'A'!C8(>7!68!5'!=&&8:%=6'7!L%6 ;!@%A(&'&!:=(&%>!=!L%7'! !!JefA=><'!8C!;8&6&!U7=6=!>86!&;8L>ZM!Q%A=)!:8>6%<&!+8&6 !&%+%)=A!68!6;8&'!%>C':6%>O!C%&;O! =>7!&;A%+B!L%6;!=!>86=5)'!&%+%)=A%6#!L%6;!A'C'A'>:' !&'D('>:'&!L'A'!C8(>7O!L;%:;!L'A'! A')=6'7!68!&%<>%C%:=>6!B(5)%:!;'=)6;!BA85)'+&!8A!7% A':6!':8>8+%:!%+B=:6!7('!68!A'7(:6%8>&! %>!C%&;'A%'&!=>7!=D(=:()6(A'!BA87(:6%8>!UT%<(A'!XMX O!2=5)'!XMKZM ! 175 Figure 6.6. 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