RefinedSystematicsoftheGenus Rhodococcus BasedonWholeGenome Analyses
VartulSangal,MichaelGoodfellow,AmandaL.Jones,RobertJ.Seviour, andIainC.Sutcliffe
Contents
1HistoricalPerspectiveandRecentDevelopmentsintheTraditionalClassification ofRhodococci .................................................................................2
2Reclassificationof R.equi as Prescottellaequi ..............................................5
3IstheName Rhodococcus Zopf1891 “Legitimate”?........................................7
4InsightsfromPhylogenomicAnalyses.......................................................7
5ConcludingComments.......................................................................17
References .........................................................................................17
Abstract Thegenus Rhodococcus hashadalongandcomplicatedtaxonomic history.Withtheadventof16SrRNAgenesequenceanalysesand,subsequently, wholegenome-basedphylogenomicstudies,theheterogeneitywithinthegenushas becomeprogressivelymoreapparentandbetterresolved.Weherereviewrecent advancesinthesystematicsofthegenus,whichcurrentlycontainsmorethan 50describedspecies.Importantdevelopmentsincludetheproposedreclassifications of Rhodococcusequi and Rhodococcuskunmingensis intonovelgeneraas Prescottellaequi and Aldersoniakunmingensis,respectively.Notably, phylogenomicstudiesconsistentlyresolvethegenus Rhodococcus intomultiple species-groupsofcoherentcompositionwhichthuslikelymeritseparategenusstatus alongside Rhodococcus sensustricto.Inparticular,awell-sampledgroupofplantassociatedspeciesweheredefineasthe “Rhodococcusfascians assemblage” likely representsanovelgenus.
V.Sangal·A.L.Jones·I.C.Sutcliffe(*)
FacultyofHealthandLifeSciences,DepartmentofAppliedSciences,NorthumbriaUniversity, NewcastleuponTyne,UK
e-mail: iain.sutcliffe@northumbria.ac.uk
M.Goodfellow
SchoolofNaturalandEnvironmentalScience,UniversityofNewcastle,NewcastleuponTyne, UK
R.J.Seviour
DepartmentofMicrobiology,LaTrobeUniversity,Bundoora,VIC,Australia
© SpringerNatureSwitzerlandAG2019
H.M.Alvarez(ed.), BiologyofRhodococcus,MicrobiologyMonographs16, https://doi.org/10.1007/978-3-030-11461-9_1
Therhodococciareremarkableorganisms:interestintheirecologyandbiological activities(andthepathogenicityofsomestrains)hassustainedthousandsofscientificstudies,includingwhatisnowtwoeditionsofthismonograph(Alvarez 2010, 2018).Consequently,itisallthemoreremarkablethatwehaven’tyetanswered definitivelythequestion “aretheyallactuallyrhodococci”?Thischapterwillreview progressinclarifyingthesystematicsofthegenus Rhodococcus inthelightofnew knowledgeandwillprovideaconvincinganswertothatquestion.
1HistoricalPerspectiveandRecentDevelopments intheTraditionalClassificationofRhodococci
Thelongandintricatetaxonomichistoryofthegenus Rhodococcus hasbeenthe subjectofseveralcomprehensivereviews(BousfieldandGoodfellow 1976; GoodfellowandWayne 1982;Goodfellowetal. 1998;GürtlerandSeviour 2010) andhencewillonlybeconsideredbrieflyhere.ThegenuswasproposedbyZopf (1891)fortwospeciesofred-colouredbacteriathathadbeenclassifiedinthegenus Micrococcus byOverbeck(1891).Earlyclassificationsbaseduponformandfunctionaredifficulttonavigateas “rhodococci” wereassignedto11genera,including Bacillus,Micrococcus, Mycobacterium and Nocardia.Thereintroductionofthe epithet “rhodochrous” formembersofthisextensivetaxonomicdiasporabyGordon andMihm(1959)representedanimportantmilestoneinrhodococcalsystematicsas thestrainsbelongingtothistaxonwereconsideredtorepresentadefinitivespecies, albeitonethatwastentativelyclassifiedinthegenus Mycobacterium.However,it soonbecameapparentfromasuccessionofstudiesbasedonchemotaxonomicand numericalpheneticmethodsthatthistaxonmeritedgenericstatus(Bousfieldand Goodfellow 1976).Followinganextensivenumericaltaxonomicstudyby GoodfellowandAlderson(1977),thegenus Rhodococcus wasreintroducedfor “rhodochrous” strainswith Rhodococcusrhodochrous (Zopf 1891)Tsukamura 1974asthetypespecies,alongwithnineadditionalspecies.Severalofthelatter havesincebeenassignedtothegenus Gordonia (http://www.bacterio.net/ rhodococcus.html).
Thetaxonomicstatusofmostofthe32validlynamed Rhodococcus species consideredbyGürtlerandSeviour(2010)andinthecurrenteditionof Bergey’ s ManualofSystematicBacteriology (JonesandGoodfellow 2012)isunderscoredby acombinationofgenotypicandphenotypicdata,althoughitisclearfromassociated 16SrRNAgenesequencestudiesthatthegenusisheterogeneous.Indeed,Jonesand Goodfellow(2012)assignedthetypestrainsof30rhodococcalspeciestothree lineages,the Rhodococcusequi, Rhodococcuserythropolis and R.rhodochrous subclades.Similarintra-genericstructurewasalsoevidentinotherstudies,although thepositionof R.equi strainstendedtobeunstable(Raineyetal. 1995;Goodfellow etal. 1998;McMinnetal. 2000;Gürtleretal. 2004;GürtlerandSeviour 2010).At thetimeofpublicationofGürtlerandSeviour(2010),thegenuscontained32validly
namedspecies.Sincethen,anadditional22 Rhodococcus specieswitheithervalidly oreffectivelypublishednameshavebeendescribed(Table 1).Inadditiontothe descriptionofthesenewspecies,ithasalsobeendemonstratedthatthebiotechnologicallyimportantstrain Rhodococcus sp. RHA1(Yametal. 2011;Cenicerosetal. 2017)belongstothespecies Rhodococcusjostii (Jonesetal. 2013a),whereas Rhodococcusjialingiae isalatersynonymof Rhodococcusqingshengii (Táncsics etal. 2014).Furthermore,recentgenomesequencedatahavebeenusedtoemendthe descriptionsof23rhodococcalspecieswithmoreprecisemeasuresofgenomicDNA G+Ccontentandestimatedgenomesizes(Nouiouietal. 2018).
Itisevidentfrom16SrRNAgenesequenceanalyses(asexemplifiedinFig. 1) thatthetypestrainsofmostofthesespeciescanbeassignedtoseveralmultimemberedcladesthatcorrespondtoasistercladethatencompassesrepresentative Nocardia typestrains.Genotypicdataacquiredfromtheanalysesofnucleicacids andassociatedphenotypicdatafromchemotaxonomicandotherexpressedfeatures (polyphasictaxonomy)hasledtoconsiderableimprovementsintheclassificationof rhodococciandothermycolicacidcontainingActinobacteriaclassifiedintheorder Corynebacteriales (GoodfellowandJones 2012).Nevertheless,problemsremain, notablythedifficultyofdistinguishingbetweengenerawithinthistaxonand betweencloselyrelatedspecieswithinindividualgenera(GoodfellowandJones 2012;Baeketal. 2018).16SrRNAgenesequenceanalysisinparticularhasplayed animportantroleinimprovingtheclassificationofthegenusalthoughitisequally clearthatthismarkerlackssufficientresolutionfordistinguishingbetweenclosely relatedtaxa.Classi ficationsbasedonwholegenomesequencesandassociated bioinformaticmethodsareprovingtobeeffectivewaysofaddressingsuchchallenges,astheyarebaseduponmassivelyexpandedamountsofsequencedata, therebyprovidingastepchangenotonlyininformationbutalsoinreliability (Sangaletal. 2014b;Whitman 2014;Chunetal. 2018;Baeketal. 2018).However, itisimportantthatwholegenomesequence-basedclassifications(phylogenomics; seebelow)adheretobothminimalstandardsforsequencingquality(Chunetal. 2018)andsoundtaxonomicpractices,suchastheneedtofollowthenomenclatural typeconceptandtherequirementtodeposittypestrainsinaminimumoftwopublic collectionsindifferentcountries(Parkeretal. 2019).
Inadditiontotheapplicationofwholegenomesequenceanalysistosystematics, futureimprovementstotheclassificationandidentificationofrhodococciwilllikely alsoderivefromtherefinementandimplementationofmatrix-assistedlaserdesorptionionisation-timeof flight(MALDI-TOF)massspectrometrymethodsforrapidly phenotypingbacteria(Hsuehetal. 2014;SchumannandMaier 2014;Pasciaketal. 2015;deAlegriaPuigetal. 2017).TheintegrationofphylogenomicandhighthroughputMALDI-TOF-basedapproacheshasmuchpotentialformicrobialsystematicsgenerally(Ramasamyetal. 2014)andinapplicationtotherhodococciand relativesspeci fically.
Table1
Rhodococcus speciesdescribedsince2010
Name Type strain 16SrRNA accession numberSourceReference
Rhodococcus artemisiae YIM 65754T
Rhodococcus nanhaiensis SCSIO 10187T
Rhodococcus canchipurensis
GU367155Endophyteof Artemisia annua L. Zhaoetal. (2012)
JN582175SouthChinaSeasedimentLietal. (2012)
MBRL 353T JN164649Limestonequarry,IndiaNimaichand etal.(2013)
Rhodococcus cerastii C5T FR714842Phyllosphereof Cerastium holosteoides Kämpfer etal.(2013)
Rhodococcus trifolii T8T FR714843Phyllosphereof Trifolium repens
Rhodococcus defluvii
Ca11T
Rhodococcus enclensis NIO1009T
Rhodococcus kronopolitisa NEAUML12T
Rhodococcus biphenylivorans
KC788572Bioreactorwastewater, Germany Kämpfer etal.(2014)
HQ858009Marinesedimentsample, Goa Dastager etal.(2014)
KF887492 Kronopolitessvenhedind Verhoeff Liuetal. (2014)
TG9T KJ546454Polychlorinatedbiphenylcontaminatedsediment, China Suetal. (2015)
Rhodococcus soli DSD51WT KJ939314Parksoil,JapanLietal. (2015)
Rhodococcus aerolatus PAMC 27367T
Rhodococcus agglutinans CFH S0262T
Rhodococcus lactis
KM044053Rainwaterfromabovethe BeringSea Hwangetal. (2015)
KP232908Soilsample,VietnamGuoetal. (2015)
DW151BT KP342300Dairywastesludge,IndiaSinghetal. (2015)
Rhodococcus antrifimi D7-21T LN867321Driedbatdung,SouthKoreaKoetal. (2015)
Rhodococcus degradans CCM 4446T
JQ776649Pollutedsoil,Switzerland Švecetal. (2015)
Rhodococcus pedocola UC12T KT301938Foresttopsoil,SouthKoreaNguyenand Kim(2016)
Rhodococcus humicola UC33T KT301939Foresttopsoil,SouthKorea
Rhodococcus sovatensis H004T KU189221Hypersalineand heliothermallakewater, Romania Táncsics etal.(2017)
Rhodococcus gannanensis M1T NR_152643Rootendophyteof Helianthusannuus L. Maetal. (2017)
Rhodococcus olei Ktm-20T MF405107Oil-contaminatedsoil,NepalChaudhary andKim (2018) (continued)
Table1 (continued)
Name Type strain
Rhodococcus psychrotoleransa CMAA 1533T
Rhodococcus electrodiphilus
JC435T
Rhodococcus daqingensisa Z1T
16SrRNA accession numberSourceReference
KY317932Rhizosphereof Deschampsia antarctica Silvaetal. (2018)
LT630357MarinecoralreefRamaprasad etal.(2018)
MH205096Petroleum-contaminatedsoilWangetal. (2018)
aEffectivelypublishednameatthetimeofwriting
2Reclassificationof R.equi as Prescottellaequi
Basedon16SrRNAgenetrees,itisnowclearthat R.equi representsadistinct phylogeneticlineage,althoughasnotedaboveitspositionisunstablewithregardto othermembersofthegenus Rhodococcus.Indeed,GürtlerandSeviour(2010)noted that “whether R.equi shouldcontinuetobeplacedinthegenus Rhodococcus or movedtoaseparateoralternativeexistinggenusstillawaitsresolution”,whileJones andGoodfellow(2012)raisedthequestionasto “whetheritshouldberecognizedas agenusinitsownright ”.Thismatterwasaddressedwiththeproposed reclassificationof R.equi asthetypespeciesofthegenus Prescottia (Jonesetal. 2013b),althoughtherulesofnomenclaterequiredthatitwasnecessarysubsequently toproposethereplacementoftheillegitimategenusname Prescottia with Prescottella (Jonesetal. 2013c),withthetypespecies Prescottellaequi.The justificationforthereclassi ficationwasbaseduponextensivephylogenetic,molecular fingerprintingandnumericaltaxonomicanalyses(Jonesetal. 2013b),which havesincebeensupportedbyphylogenomicdata(Sangaletal. 2016;seebelow). However,thequestionofthecorrectnomenclaturehasbeencomplicatedbythe formalreclassificationof R.equi intothespecies Rhodococcushoagii (Kämpfer etal. 2014).Thismovehasbeenchallengedina “RequestforanOpinion” fromthe JudicialCommissionoftheInternationalCommitteeonSystematicsofProkaryotes, whichrequestedtheretentionofthespeciesepithet equi (Garrity 2014).Untilsuch anOpinionisissued,thecorrectnameofthetaxonremains R.hoagii,andthespecies name P.equi cannotbevalidated.AsreviewedinGoodfellowetal.(2015),a pragmaticsolutionistorefertotheorganismas “Rhodococcusequi (Rhodococcus hoagii/Prescottellaequi)” at firstusageinscienti ficcommunications,whilethe matterisunderconsiderationbytheJudicialCommission.Wenotethatthecommunitycanuseanyofthesenamesalthoughcurrently R.hoagii isthe “correct” one (Tindall 2014a).
While16SrRNAgenesequenceanalysisrecovered26 R.equi strainsinasingle cluster,themolecular fingerprintingandnumericaltaxonomicanalysesofJones etal.(2013b)suggestedthatthespeciescouldberesolvedintotwosubclusters. However,subsequentgenomicanalysishasindicatedahighdegreeofrelatedness
Fig.1 16SrRNAgene
sequenceanalysisof membersofthegenus
Rhodococcus and representativesofrelated generaintheorder Corynebacteriales.Thetree wasconstructedusingthe neighbour-joiningalgorithm inMEGA.Nodessupported bygreaterthan50%of1000 bootstrapreplicationsare indicated.NodeslabelledL orPwerealsosupportedin themaximumlikelihoodor maximumparsimonytrees, respectively.Nodeslabelled *weresupportedbyallthree tree-makingalgorithms
Rhodococcus biphenylivorans TG9T (KJ546454)
Rhodococcus lactis DW151BT (KP342300)
Rhodococcus pyridinovorans PDB9T (AF173005)
Rhodococcus gordoniae W 4937T (AY233201)
Rhodococcus rhodochrous ATCC 13808T (X79288)
Rhodococcus artemisiae YIM 65754T (GU367155)
Rhodococcus coprophilus CUB 687T (X80626)
Rhodococcus phenolicus G2PT (AY533293)
Rhodococcus zopfii T1T (AF191343)
Rhodococcus ruber CIP 104180T (X80625)
Rhodococcus aetherovorans 10bc312T (AF447391)
Rhodococcus electrodiphilus JC435T (LT630357)
Rhodococcus aerolatus PAMC 27367T (KM044053)
Rhodococcus rhodnii N445T (X80621)
Rhodococcus triatomae CCUG 50202T (AJ854055)
Rhodococcus corynebacterioides ATCC 14898T (AF430066)
Rhodococcus trifolii T8T (FR714843)
Rhodococcus enclensis NIO-1009T (HQ858009)
Rhodococcus kroppenstedtii KO7-23T (AY726605)
Rhodococcus olei Ktm-20T (MF405107)
Rhodococcus canchipurensis MBRL 353T (JN164649)
Rhodococcus gannanensis M1T (KX887333)
Rhodococcus antrifimi D7-21T (LN867321)
Rhodococcus defluvii Ca11T (KC788572)
Rhodococcus humicola UC33T (KT301939)
Rhodococcus pedocola UC12T (KT301938)
Rhodococcus cerastii C5T (FR714842)
Rhodococcus cercidiphylli YIM 65003T (EU325542)
Rhodococcus fascians ATCC 12974T (X79186)
Rhodococcus yunnanensis YIM 7056T (AY602219)
Rhodococcus kyotonensis DS472T (AB269261)
Rhodococcus sovatensis H004T (KU189221) "Rhodococcus psychrotolerans" CMAA 1533T (KY317932)
Rhodococcus opacus ATCC 51881T (X80630)
Rhodococcus percolatus MBS1T (X92114)
Rhodococcus jostii NBRC 16295T (AB046357)
Rhodococcus marinonascens 3438WT (X80617)
Rhodococcus koreensis DNP505T (AF124342)
Rhodococcus imtechensis RKJ300T (AY525785)
Rhodococcus wratislaviensis N805T (Z37138)
Rhodococcus nanhaiensis SCSIO 10187T (JN582175) “Rhodococcus daqingensis” Z1T (MH205096)
Rhodococcus maanshanensis M712T (AF416566) "Rhodococcus kronopolitis" NEAU-ML12T (KF887492)
Rhodococcus tukisamuensis Mb8T (AB067734)
Rhodococcus globerulus R58T (X80619)
Rhodococcus erythropolis N11T (X79289)
Rhodococcus degradans CCM 4446T (JQ776649)
Rhodococcus baikonurensis A1-22T (AB071951)
Rhodococcus jialingiae djl-6-2T (DQ185597)
Rhodococcus qingshengii djl-6T (DQ090961)
Rhodococcus kunmingensis YIM 45607T (DQ997045)
Rhodococcus agglutinans CFH S0262T (KP232908)
Rhodococcus soli DSD51WT (KJ939314) “Rhodococcus equi” ATCC 6939T (X80614)
Rhodococcus hoagii ATCC 7005T (X82052)
Nocardia nova NBRC 15556T (AF430028)
Nocardia pseudovaccinii DSM 43406T (AF430046)
Nocardia vaccinii ATCC 11092T (AF430045)
Nocardia beijingensis AS4.1521T (AF154129)
Nocardia pneumonia IFM 0784T (AB108780)
Nocardia farcina ATCC 3318T (Z36936)
Nocardia kroppenstedtii N1286T (DQ157924)
Nocardia abscessus IMMIB D-1592T (AF218292)
Nocardia asteroides ATCC 19247T (AF430019)
Nocardia iowensis UI 122540T (DQ925490)
Nocardia speluncae N2-11T (AM422449)
Segniliparus rotundus CDC 1076T (CP001958)
Smaragdicoccus niigatensis Hou_blueT (AB243007)
Tomitella biformata AHU1821T (AB491283)
Millisia brevis J18T (AY534742)
Skermania piniformis ATCC 49497T (Z35435)
Williamsia muralis MA140/96T (Y17384)
Gordonia bronchialis ATCC 25592T (CP001802)
Gordonia sputi ATCC 29627T (X80634)
Gordonia malaquae IMMIB WWCC-22T (AM406674)
Gordonia phosphorivorans Ca8T (HE574551)
Dietzia maris ATCC 35013T (X79290)
Tsukamurella paurometabola ATCC 8368T (CP001966)
Tsukmurella pulmonis IMMIB D-1321T (X92981)
Amycolicicoccus subflavus DQS3-9A1T (EF564379)
Hoyosella altamirensis OFN S31T (FJ179485)
Mycobacterium koreense 01-305T (JF271826)
Mycobacterium chelonae subsp. chelonae CM 6388T (AY457072)
Mycobacterium fortuitum subsp. fortuitum ATCC 6841T (AY457066)
Mycobacterium porcinum E10241-1T (AY457077)
Mycobacterium mucogenicum MO76T (AY457074)
Mycobacterium parafortuitum ATCC 19686T (X93183)
Mycobacterium rufum JS14T (AY943385)
Mycobacterium wolinskyi M739T (AY457083)
Mycobacterium hiberniae Hi 11T (X67096)
Mycobacterium elephantis CIP 106831T (AJ010747)
Mycobacterium madagascariense P2T (AB537170)
Mycobacterium noviomagense CIP 109766T (EU239955)
Mycobacterium shimoidei ATCC 27962T (AJ005005)
Mycobacterium intermedium ATCC 51848T (X67847)
Mycobacterium parmense MUP 1182T (AF466821)
Mycobacterium africanum ATCC 25420T (AF480605)
Mycobacterium microti ATCC 19422T (AF480584)
Mycobacterium bovis subsp. bovis ATCC 19210T (AF547903)
Mycobacterium tuberculosis subsp. tuberculosis H37RvT (X58890)
Corynebacterium diphtheria ATCC 27010T (X84248)
Corynebacterium glaucum IMMIB R-5091T (AJ431634)
Corynebacterium imitans ATCC 700354T (Y09044)
Corynebacterium afermentans subsp. afermentans ATCC 51403T (X82054)
Corynebacterium appendicis CCUG 48298T (AJ314919)
Corynebacterium auris ATCC 51966T (X81873)
Corynebacterium camporealensis CRS-51T (Y09569)
Corynebacterium confusum CCUG 38267T (Y15886)
Corynebacterium massiliensis CCUG 53857T (EF217056)
Corynebacterium accolens CNCTC Th1/57T (AJ439346)
Corynebacterium aurimucosum CCUG 47449T (AJ309207)
Corynebacterium minutissimum ATCC 23348T (X84678)
Turicella otitidis ATCC 51513T (X73976)
betweenstrainsof R.equi (Sangaletal. 2014a, 2016;Anastasietal. 2016), indicativeofaclonalpopulation,althoughsixsub-cladeswereevident(Anastasi etal. 2016).Similarly,amultilocussequencetypingschemefor R.equi basedon sevenhousekeepingloci(https://pubmlst.org/rhodococcus/)supportedaclonalpopulationstructureandidentified37sequencetypeswithinthespecies,16ofwhich couldbegroupedinto6clonalcomplexes(Duquesneetal. 2017).
3IstheName Rhodococcus Zopf 1891 “Legitimate”?
Apartfromtheabovecomplicationsregardingthenomenclatureof R.equi,Tindall (2014b)hasreportedthatthegenusname Rhodococcus Zopf 1891 isillegitimate undertherulesofnomenclaturalpriorityintheInternationalCodeofNomenclature ofProkaryotes(Parkeretal. 2019),asitpost-datestheestablishmentofthealgal genus Rhodococcus Hansgirg1884.However,thealgalgenus Rhodococcus Hansgirg1884iscurrentlyregardedassynonymouswiththeearliercyanobacterial genus Chroococcus Nägeli1849(http://www.algaebase.org/search/genus/detail/? genus_id¼42893).Thus,thelegitimacy(orotherwise)ofthebacterialname Rhodococcus Zopf 1891 willultimatelydependonbothconfirmingtheassignment of Rhodococcus Hansgirg1884to Chroococcus Nägeli1849andalsooncomplex revisionstoboththeInternationalCodeofNomenclatureofAlgae,FungiandPlants (ICNafp)andInternationalCodeofNomenclatureofProkaryotesregardingwhich rulesshouldapplytocyanobacteria(Tindall 2014b;OrenandVentura 2017).Such revisionswillundoubtedlybetime-consuming,andso,inthemeantime,itseems prudentthatresearchersstudyingmembersofthecurrentgenus Rhodococcus maintaintheuseofthisnameuntilthesemattersareresolved(e.g.bytheInternationalCommitteeonSystematicsofProkaryotesanditssistercommitteesgoverning nomenclature).Ironically,thereclassi ficationofvariousrhodococcalspecies-groups intonewgenera(seebelow)willhelptoprovidethesenewtaxawithlegitimate names,solongastherulesoftheInternationalCodeofNomenclatureofProkaryotes arecorrectlyfollowed.
4InsightsfromPhylogenomicAnalyses
Gürtleretal.(2004)posedthequestion “Canwholegenomeanalysisrefinethe taxonomyofthegenus Rhodococcus?” Itisnowclearthatthisquestioncanbe answeredintheaffirmative.Fourphylogenomicstudieshavedefinedseveralrobust
species-groupswithinthegenus.Inastudyfocussedonplantpathogenicrhodococci andtheintraspeci ficstructureof Rhodococcusfascians,Creasonetal.(2014) generatedaphylogenetictreebasedonaveragenucleotideidentity(ANI)divergence for59genome-sequencedrhodococci,whichwasresolvedinto7cladeswithintragroupANIvalues >70–75%(athresholdtheyconsideredrelevanttothedelineation ofbacterialgenera).The25plant-associatedisolatesincludedwererecoveredintwo relatedclades.Eighteenoftheseisolates(includingthetypestrainof R.fascians) wererecoveredinacladewithfourrecognisablesubclades(1i–1iv).Theremaining 34rhodococcianalysedwererecoveredin fiveclades,includingClade5containing R.equi strains.However,theclusteringmethodandabsenceofoutgrouptaxa preventedrelationshipsbetweenthesecladesandothermycolicacid-containing bacteriafrombeinginferred.
Subsequently,threefurtherphylogenomicstudieshaveconfirmedtheheterogeneitywithin Rhodococcus.Inastudyfocussedonunderstandingrelationships between29 R.equi strains,Anastasietal.(2016)usedPhyloPhlAntoanalysethe genomesofthesestrains,alongwiththoseof46rhodococci(discountingasequence misattributedto “Rhodococcusrhodnii” NRRLB-16535T;seebelow)and57other genomesrepresentingstrainsbelongingto11generaoftheorder Corynebacteriales . Thegenomeof Streptomycesalbus NBRC1304T wasusedastheout-group.This analysisrecoveredallthe Rhodococcus strainsinasinglelineagebutalsoidentified fivewell-supportedspecies-groupswithinthisphyleticline,fourofwhichwereeach resolvedintotwosubclusters.Contemporaneously,weusedPhyloPhlAntoanalyse 100rhodococcalgenomesand15genomesrepresentingsevengeneraoftheorder Corynebacteriales (Sangaletal. 2016).Inthisstudy,sevenrhodococcalspeciesgroupswereidentified,severalofwhichwereseparatedbylineagescontaining representativesofothergenera,i.e.indicating Rhodococcus tobeparaphyletic. SimilartoCreasonetal.(2014),wealsofoundtheANIbthresholdforseparating potentialgeneratobe~74.8%.Toexplorethisfurther,wehaveextendedour PhyloPhlAnanalysistoinclude116rhodococcalgenomesand15genomes representing7generaoftheorder Corynebacteriales (Fig. 2;Table 2).Notably, thistreenowincludesgenomesfortypestrainsof29ofthe52currentlyvalidly namedrhodococcalspecies.Thisanalysisgeneratedatreewiththesameoverall topologyasthatinSangaletal.(2016),withthe Rhodococcus strainsrecoveredin thesamesevenspecies-groups(Table 3).Inaddition, R.rhodnii strainLMG5362, whichwasconsideredtobeapossiblymisclassifiedsingletonbySangaletal. (2016),isnowshowntobelongtoanewlydefinedspecies-group(H),alongwith R.rhodnii NBRC100604T andthetypestrainof Rhodococcustriatomae (Fig. 2).As notedbyAnastasietal.(2016),agenomedepositedas “R.rhodnii NRRL B-16535T” (GenbankGCA_000720375.1)isclearlymisclassified,asitformsa lineagedistantfromtheothertwo R.rhodnii strains(Fig. 2).AsintheSangal etal.(2016)analysis, Rhodococcuskunmingensis DSM45001T wasrecoveredasa singletonlineageinFig. 2,whereasitistypicallylooselyaffiliatedwith R.equi (Prescottella)in16SrRNAgenetrees(e.g.Fig. 1).
Finally,arecentlarge-scalephylogenomicanalysisofthephylum Actinobacteria,basedon1142actinobacterialtypestraingenomes,hasalso
R. fascians A22b R. sciansfa A73a R.fascians 02-815 R.sp 29MFTsu3.1
CorynebacteriumdiphtheriaeNCTC 03529
R.rhodniiNRRLB-16535TSegniliparusrugosus ATCC BAA-974 Segniliparus r otundus DSM 44985 Williamsiasp. D3 Williamsiasp. ARP1 Gordonia KTR9 Gordonia bronchialis DSM 43247 Gordonia p o lyisoprenivorans VH2 R.sp. MEB064 R sp. UNC23MFCrub1.1 R.R.kroppenstedtiiDSM44908T coryn e bacterioides DSM 20151TR.kyotonensisJCM23211T R.yunnanens isNBRC103083T R.R.fasciansA44a R.fascians02-816c sp. 114MFTsu3.1
CorynebacteriumdiphtheriaeNCTC05011
R. phenolicus DSM 44812T R. zopfii NBRC 100606T Nocardia cyriacigeorgica GUH2 800357ATCCssiilienrasbrdiaacNo 25101MIFacinicrfaairdaNoc 15531NBRCesdasteroiaNocardi 45001TSMDssikunmingen.RgatensisiniagdicoccusSmar
R. sp . RD6 2 R. triatomae BKS 1514 R. tukisamuensis JCM 11308T R. sp. UNC363MFTsu5.1 R. maanshanensisDSM 44675T R. defluvii Ca11T R. hoagiiDSM20295TR.equi103SR.equiN1301R.equiATCC33707 R equiN1288 R.equiN1295 R.equiC7T
R.sp. B7740 R fascians05-339-1 R.sp.BS-15R.fasciansA76 scensmarinonaR. NBRC 14363T koreensisR. MDS 98T444 B4opacusR. jostiiR. 95T162NBRC 605T100NBRCaviensislwratisR. 7RopacusR. RHA1ostiijR. R. sp. JVH1 R. sp. DK17 usopacR. 30PD6imtechensisR. 300TRKJ M213opacusR. 43205TDSMopacusR. 2016IFPwratislaviensisR.
R1101 sp R R. gordoniae DSM 44689T R. rhodochrous DSM 43241T R. rhodochrous BKS6-46 R.sp. R4 RR.pyridinivoransAK37 sp. P52 R .sp. Chr-9 R. p yrid in vo r a n s S B3 0 9 4 R. pyridin ivorans DSM 44555T R. fascians A78 R. fascians A3b R. fascians LMG 3616 R. fascians LMG 3602 R fascians LMG 3623T R. fascians LMG 3605 R. fascians D188 R. sp. JG-3 R. fascians F7 R. sp. PML 026 R. fascians GIC36 R. fasci ans GIC26 A25fnsascifaR. 5623MGLsscianfa.R 164-50nssciafa.R 2A21dnsciafasR.
44881DSM atambiforllaiteomT1182AHU 3625GMLiiodnrhR. 4T00601NBRCiihodnrR. 6T11301NBRCtriatomaeR. R. rhodochrous ATCC 21198 R. aetherivorans IcdP1 R. aetherivorans BCP1 R. sp BCP1 R. sp EsD8 R. coprophilus NBRC 100603T R. ruber BKS 20-38 R. ruber Chol-4 R. ruber IEGM 231 R. ruber DSM 43338T R.sp. P14R.ruberP25
R. sp. AD45 R. sp. 4J2A2R.globerulus NBRC14531TR.R.rhodochrousNRRLB-1306 baikonurensisJCM18801R.qingshengii TUHH-12 R. rh odochrous ATCC 17895 R. erythropolis DN1 R. erythropolis BG43 R. sp. ARP2 R eryth rop olis NBR C 15567T R . e rythropolis PR4 R. ery thropolis XP R. erythropolis R138 SK121erythropolisR. oliserythropR. NRRL532-16B R.isnclenseNIO-1009T R.erythropolis JCM682422iCAS9erythropolisR. iiqingshengR. JCM 15477T R. sp. AJR001 R. sp. 311R R. qingshengii BKS 20-40 R. opacus NRRL B-24011 R. erythropolis CCM2595 R. sp. P27
Fig.2 Phylogenomicanalysisofmembersofthegenus Rhodococcus andrepresentativesofrelatedgeneraintheorder Corynebacteriales .Thegenome sequencedatawereobtainedfromtheGenBankandre-annotatedusingRASTserver(Azizetal. 2008 ).Thephylogenetictreewasconstructedfromtheprotein sequencesusingPhyloPhlAn(Segataetal. 2013 ).PhyloPhlAnextractsasubsetofaminoacidsfrom400universalproteinsandconstructsamaximum likelihoodtreefromtheconcatenatedaminoacidsequencealignment.Thescalebarshowsanormalisedfractionofthetotalbranchlengthsasdescrib edby Segataetal.( 2013 )
T LRRK000000005.1868.2B(B2)
(continued)
Rhodococcus sp.AD45JYOP010000006.7961.7D
Rhodococcus sp . 4J2A2CEDU010000006.4561.8D
Rhodococcus sp.114MFTsu3.1ARTN000000005.5564.7E(E1)
Rhodococcus sp.29MFTsu3.1ARND000000005.5864.6E(E1)
Rhodococcus sp.BS-15BAOX010000005.5164.4E(E2)
Rhodococcus sp.B7740NZ_CP010797.15.3464.9E(E2)
Rhodococcus sp.PML026JZIS010000005.1764.7E(E2)
Rhodococcus sp.JG-3AXVF000000005.2764.6E(E2)
sp.AW25M09CAPS000000005.6464.1E(E2)
sp.UNC23MFCrub1.1JMLQ010000004.768.5F
sp.MEB064JXQS010000004.6767.0F
sp.UNC363MFTsu5.1JMLO010000005.6769.3G
sp.RD6.2CVQP010000005.5768.4G
.GenomesinboldwerenotincludedintheanalysispresentedinSangaletal.(
Table3 Species-groupsevidentwithinthecurrentgenus Rhodococcus asdeterminedby phylogenomicanalyses
Representative speciesa
“
R.equi”
R.defluvii
R.ruber
R.coprophilus
R.gordoniae
R.rhodochrous
R.phenolicus
R.pyridinivorans
R.zopfii
R.imtechensis
R.jostii
R.koreensis
R.opacus
R.marinonascens
R.wratislaviensis
R.enclensis
R.erythropolis
R.qingshengii
R.globerulus
R.fascians
R.kyotoensis
R.yunnanensis
R.corynebacterioides
R.kroppenstedtii
R.maanshanensis
R.tukisamuensis
R.rhodnii
R.triatome
Speciesgroup b (Fig. 2)
Anastasi etal.(2016) clade Creasonetal.(2014) cladeb
A3a5
B11b6
B21a7
Affiliatedspecies from16SrRNA analysisc
R.agglutinans
R.soli
R.aetherivorans
R.artemisiae
R.biphenylivorans
R.lactis
C2b4
R.percolatus
D2a3
E5a1and2
R.baikonurensis
R.degradans
R.cerastii
R.cercidiphylli
R.sovatensis
F5bNotincluded R.trifolii
G3bStrainBKS-51-14 associatedwithclade 5
H4 (R.rhodnii LMG5362)
R.rhodnii LMG 5362associatedwith clade5
R.kunmingensisd SingletonNotincluded
aTheearliestdescribedspeciesisshowninbold
R.kronopolitis
R.daqingensis
bAllthesespecies-groupswerealsorecoveredaswell-separatedclustersinasevenprotein multilocussequenceanalysis(maximumlikelihoodtree)of199membersof Rhodococcus (Savory etal. 2017)
cSpecieslikelytobelongtothesameclusters/cladesasjudgedfromaconsistentaffiliationwith relatedspeciesin16SrRNAgenetrees
dNowreclassi fiedas Aldersoniakunmingensis (Nouiouietal. 2018)
confirmedthespecies-groupsindicatedinTable 3 (Nouiouietal. 2018).Whole proteomeanalysisusingtheGenomeBLASTDistancePhylogeny(GBDP)wasused todeterminebothintra-andsupra-genericrelationshipswithinthephylum.Withthe exceptionof R.kunmingensis,the29rhodococcaltypestrainsincludedwererecoveredasalineagewithinthefamily Nocardiaceae.Importantly,withinthis “core”
Rhodococcus lineage,thetypestrainswereresolvedintoeightlineagesinexact agreementwithgroupsA–HinTable 3.However,similartoFig. 2, R.kunmingensis DSM45001T wasrecoveredasasingletonwellseparatedfromanyofthesespeciesgroups,showingapoorlysupportedrelationshipwith Skermaniapiniformis .Consequently,Nouiouietal.(2018)haveproposedthereclassificationof R.kunmingensis DSM45001T asthetypespeciesrepresentinganovelgenus, Aldersoniakunmingensis gen.nov.,comb.nov.
Itisnotablethatalloftheabovephylogenomicanalysesrecoverwell-supported species-groupsofverysimilarcomposition(Table 3). R.equi strains,alongwiththe typestrainof R.defluvii,arerecoveredinawell-separatedgroupcorrespondingto theproposedgenus Prescottella (Jonesetal. 2013b, c;Sangaletal. 2015, 2016). GroupB(Fig. 2)containsthetypestrainof R.rhodochrous,thetypespeciesofthe genus,andcanthereforebedefinedas Rhodococcus sensustricto.Theformal proposalofnovelgenerainadditionto Aldersonia and Prescottella mayrequire furtheranalyses(notablyofgenomesofasyetunsequencedrhodococcaltype strains).However,itisalreadyevidentthatGroupE(Fig. 2)containingsoiland plant-associatedstrainsrelatedtothe R.fascians (Clades1and2sensuCreasonetal. 2014)shouldbereclassifiedintoatleastonenovelgenuscontaining R.fascians, Rhodococcuskyotonensis, Rhodococcusyunnanensis andmultiplenovelspecies (Creasonetal. 2014;Sangaletal. 2016).Indeed,multilocussequenceanalysis combinedwithANIanalysesofalargercollectionofplant-associatedstrainsthat mapontoGroupEindicatedthatClades1and2maycontainatleast13novel speciesinadditionto R.fascians (Savoryetal. 2017).Fornow,werefertothese strainsasthe R.fascians assemblage.ItisnotablethatSavoryetal.(2017)also concludedthatthisgroupingcontains R.kyotonensis andiswellseparatedfrom otherrhodococci(R.yunnanensis wasnotincludedintheiranalysis).Their multilocussequenceanalysisof199 Rhodococcus strains(basedontranslated sequencesfor ftsY, infB, rpoB, rsmA, secY, tsaD and ychF)yieldedamaximum likelihoodtreewithmajorgroupingsstrikinglyconcordantwithGroupsA–Hin Table 3 andalsohighlightedthedistantrelationshipof R.kunmingensis DSM 45001T totherhodococci.
Itisevidentfromtheabove,andTable 3,thatseveralindependentresearchgroups usingdifferingphylogenomicmethodologieshavealldelineatedatleasteightgroups ofspeciescurrentlyclassifiedinthegenus Rhodococcus,asidefromthe reclassificationof R.kunmingensis intothegenus Aldersonia (Nouiouietal. 2018). Asexpandingouranalysisfrom100to116strains,mostlywithgenomedatafortype strains,hasnotaddedtothenumberofclustersidentifiedwithinthegenus,itislikely thatasfurtherstrainsaresequencedandanalysedtheywill fitmainlyintotheeight species-groupsdefinedinTable 3.Indeed,theconsistentassociationin16SrRNA genesequencetrees(e.g.Fig. 1)ofsomespeciesthathaveyettohaverepresentative genomessequencedwithtaxaalreadyassignedtospecies-groupsA–Hstrongly predictsthatthesespecieswilleventuallybeassignedtothecorrespondinggroups (Table 3).Forexample,16SrRNAgeneanalyses(e.g.Guoetal. 2015;Lietal. 2015; ChaudharyandKim 2018;Fig. 1)consistentlyindicatethat Rhodococcus agglutinans and Rhodococcussoli areprobablymembersofthegenus Prescottella.
Similarly,16SrRNAgeneanalyses(e.g.Silvaetal. 2018;Táncsicsetal. 2017) consistentlyassociate Rhodococcuscerastii , Rhodococcuscercidiphylli and Rhodococcussovatensis with R.fascians, R.kyotonensis and R.yunnanensis,asin Fig. 1.
5ConcludingComments
Clearly,remarkableprogresshasbeenmaderecentlyinresolvingthecomplex systematicsofthegenus Rhodococcus,inparticularthroughtheapplicationof phylogenomicapproaches.Theheterogeneitywithinthegenusisconfirmedand theseparationoftwopathogenicspeciesintothegenus Prescottella (associatedwith animalhosts)andthe R.fascians assemblage(plant-associated)isespeciallynotable. Awealthofgenomicdataarenowavailableforrhodococcalstrains,includingmore than50%ofthecurrentlyrecognisedtypestrains.Completionofgenomesequencingdatafortheremainingrhodococcaltypestrainswillnodoubtbringfurther insightsintothegroupingsdescribedherein(Table 3),alongwithimportantinsights intotheirbiologyanddefiningcharacteristics.Thedivisionof Rhodococcus into multiplegeneramaybeconsideredcontroversialasonepersons’ phylogenomically definedgenusisanother ’sintra-genus “species-group”.Nevertheless,thetaxonomic statusof Rhodococcus seemstobecurrentlypoisedlikeagameofJenga:once blockssuchas Aldersonia, Prescottella andthe R.fascians assemblagehavebeen moved,thetowerwilltumbleintomultiplegenera,aswasthecasewiththeaerobic endospore-formingbacilliand,morerecently, Mycobacterium (Guptaetal. 2018). Thus,itseemslikelythatafutureeditionofthismonographwillneedtobecalled “Biologyof Rhodococcus, Prescottella andcloselyrelatedgenera”
References
AlvarezHM(2010)Biologyof Rhodococcus.Springer,Heidelberg
AlvarezHM(2018)Biologyof Rhodococcus.Springer,Heidelberg
AnastasiE,MacarthurI,ScorttiM,AlvarezS,GiguereS,Vazquez-BolandJA(2016)Pangenome andphylogenomicanalysisofthepathogenicactinobacterium Rhodococcusequi.GenomeBiol Evol8:3140–3148
AzizRK,BartelsD,BestAA,DejonghM,DiszT,EdwardsRA,FormsmaK,GerdesS,GlassEM, KubalM,MeyerF,OlsenGJ,OlsonR,OstermanAL,OverbeekRA,McneilLK,PaarmannD, PaczianT,ParrelloB,PuschGD,ReichC,StevensR,VassievaO,VonsteinV,WilkeA, ZagnitkoO(2008)TheRASTServer:rapidannotationsusingsubsystemstechnology. BMCGenomics9:75
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Gazette, Edinburgh, newspaper commenced by Captain Donaldson, 212; recommenced, 324.
G , William, invents stereotyping, 555; his son James joins the rebellion, 557.
Gentleman, John Purdie pleads that he is not a, 352.
G of Durie and his colliers, 249.
—— of Linkwood, imprisoned in Elgin tolbooth, and burns it, 239.
Gilmerton, subterranean house at, 502.
Gipsies of the province of Moray, 233.
Girded Tails, 448.
Glasgow, cruelty at to Quakers, 57; rise of commercial wealth in, 125; trades with colonies, 431; deterioration of morals at, 486; mercantile losses at, 337, 487, 565; bankrupt pilloried, 487; malt-tax riot at, 508; making great advances, 515; a mad merry-making at, 543; afflicted with bugs, 542.
Glass for mirrors, art of polishing, by Leblanc, a French refugee, 154.
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G , Gordon of, attempt to assassinate him, 488.
G , Lady, dispute between her and her eldest son, 159.
Glencoe, massacre at, 2, 62; French version of, 64.
Glenorchy, Episcopal minister of kept in at the Revolution, 7.
G , Duchess of (Elizabeth Howard), meeting of Catholic worshippers at her house in the Canongate, 466.
G , Duchess of (Elizabeth Mordaunt), introduces agricultural improvements, 419; pensioned for Protestantising her husband’s family, 554.
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G of Monymusk’s improvements of land, 418.
G , Captain, and his companions, unjustly tried and executed, 316.
G , Rev. James, Episcopal minister, persecutions of, 350.
G , Professor, his machine for raising water, 237.
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accused of ‘clipping and coining,’ 145.
Gunpowder, explosion at Leith, 264.
H , Thomas, Earl of, his improvements and plantations, 417.
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H , Lady Anne, her funeral, 212.
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H , Lord Basil, his death, 246.
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H ’ lottery, 88.
H , Rev. James, a noted clergyman of Edinburgh, 397, 429.
Harvest of 1699, thanksgiving for, 221.
Haunted houses, 169, 435.
Healing virtues ascribed to crystal, ivory, stones, glass, &c., 262; Dow Loch, 263.
Healths, treasonable, 182.
Hell-fire clubs, 521.
H , John, persecuted for preaching without authority, 149.
Heraldry, Alexander Nisbet’s System of, published by aid from Scottish parliament, 276.
Heriot’s Hospital boys taught useful arts at the suggestion of ‘Society of Improvers,’ 530.
Hership of cattle on lands of Lord Rollo, 117.
Highlanders, predatory habits of the, 30, 31, 498, 612.
Highlands, resistance in, to taxation, 91; ignorance in, 252.
Highway robberies, 83.
Historia Anglo-Scotica, a book, burned at the Cross of Edinburgh, 276.
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Holyrood Sanctuary, anecdotes of the, 349.
H , Earl of, ordered into Edinburgh Castle as a dangerous person, but allowed, on medical certificate, to remain at home, 117.
H , Lady, of Renton, conduct at her husband’s funeral, 200.
H of Renton writes about increase of witchcraft, 94; affray with tenants of Sir James Hall of Dunglass, 345.
Hoops for ladies, fashionable in 1719, 448.
H of Rankeillor, an agricultural improver, 485.
H , Charles Hope of, his arrangement for supplying victual to his miners, 210; his windmill at Leith, 290.
‘Horn Order,’ meeting called the, 482.
Hospital for sick first established in Edinburgh, 557.
Hospitality, great, in Scotland, 570.
Housebreaking, capitally punished by the Lord Provost of Edinburgh in 1730; W. Muir’s execution, 568.
H , James, and Sir J S of Greenock, assault between, 402.
H , David, circumstances connected with his birth, 56.
H , John of Ninewells, married to Lady Falconer, 55.
H of Marchmont, 1.
Hummum, a, or Turkish bath, set up at Perth in 1702, 260.
H and S hanged for forgery, 335.
Hunters’ ball at Holyrood, 590.
Hurricane in January 1739, 603.
Husbands ill-using wives, their punishment by the Stang, 589.
I , Earl of, admitted as an extraordinary Lord of Session, 341; curious anecdotes of in connection with the Post-office, 266.
Immorality and impiety ascribed to Scotland by General Assembly in 1691, 41; efforts to restrain, 342.
Improvers [Agricultural] Society of, 484, 580.
Incestuous connections severely treated, 59, 354.
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Infanticide and concealed pregnancy, 26.
Infirmary at Edinburgh, its origin, 557.
Influenza in Scotland, 554.
Inoculation introduced into Scotland, 530.
Insurance against fire, 446.
Intelligence-office projected, 244.
Inventions and manufactures, various, 154.
Inverary petitions for ‘ease’ from the tax-roll, pleading ‘poverty and want of trade,’ 51.
Invergarry House garrison, 304.
Inverlochy, fort planted at, 2.
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I of Drum, of weak intellect, arrangements regarding, 22;
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I of Murtle’s conduct towards Lady of Drum, 144.
I , Robert, murders his two pupils, 423.
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Jacobite party formed, 2;
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J , Joseph, Baculator of Damascus, in Edinburgh, 581.
J VII., death of, 107.
Jedburgh, incident at proclamation of King William at, 7.
J , James, a very wretched prisoner, 14.
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K , Laird of, amounts paid for his daughter’s education, 57.
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K ’ Disfigured Pictures, an optical curiosity, 101.
Kirkcaldy, &c., nearly ruined by the debts of a regiment quartered there, 45.
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Ladies, Scottish, in 1718, described by a traveller, 433.
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Lanark, assisted on account of poverty, in building a bridge, 134.
Land Mint, essay published on, 320.
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Lantern, Magical, in 1694, 100.
L , Bailie, of Haddington, imprisoned, 33.
L , John, of Croshlachie’s maltreatment, 157.
L , French refugee, mirrors made by, 154.
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Levellers of Galloway, 492.
L , Earl of, assaulted by Boswell of Balmouto, 84; by revellers, 312; carries Excise money to London, 340.
Libraries, presbyterial, in the Highlands projected, 250; partly realised, 253.
Licentiousness, 41, 320; proclamations regarding, 342.
L , Patrick, upholsterer, connected with nobility, 547.
Linen manufacture, 85, 541.
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L , Hugh Lord, confined at the Revolution, 11.
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Loyalty a paradoxical feeling, 415.
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M D of Barrisdale, 616.
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M‘E , James, starts a newspaper, 439.
M‘F , a drover, robbed, 83.
M‘F , Mrs, murders Captain Cayley, 412.
M‘G , Mr, minister of Kinross, his house haunted, 435.
M , Robert (Rob Roy), see R R .
M of Glengyle levies black-mail, 612.
M , William, a fencing-master, 267.
M , General, his cheap dinner, 46.
M , Roderick, of Prestonhall, his petition for transporting victual from Forfarshire to Midlothian, 211.
M , Sir George, warrant granted to print his works, 220.
M , Andrew, his house haunted, 109.
M , Laird of, kept out of his property in Glenroy, 15;
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M‘L , John, sentenced to be whipped and banished for tampering with recruits, 79.
M , Professor Colin, election of, 512.
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M of Invernahaven charged with stealing cattle from Grant of Conygass, 142.
M of Pall-a’-chrocain kills the last wolf in Scotland, 609.
M , James, a Quaker, pressed as a soldier, 59.
M ’ , Governor, return to Scotland, 585.
Magazine, Scots, established, 603.
Malicious Society of Undertakers, 578.
Malt, Patrick Smith’s plan for drying, 303.
—— tax riots at Glasgow, 508.
Manners, general change of (1730), 568; levity of, censured, 520.
Man-stealing, a case of, 44; edict against, 211.
Manufactures set up, 85, 126, 154.
M , Earl of, hoists standard of rebellion in Aberdeenshire, 389; letter to Robertson of Struan, 526.
Marriages, forbidden, 353.
Marriages in high life, ceremonies at, 240.
Marrow Controversy, 441.
M ’ description of Western Isles, 278.
Martyrs’ tomb in Greyfriars’ Churchyard, 533.
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M , Robert, a noted early writer on agriculture, 485.
M of Dargavel and H of Orbieston, dispute between, 69.
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Medical practice, popular, as exhibited in Tippermalloch’s Receipts, 53; fees, 22, 117.
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Mercantile enterprise in Scotland takes its rise, 121; increased after the Union, 336.
Merchandising Spiritualised, a book printed in Glasgow in 1699, 220.
Merchant Company of Edinburgh, their treatment of Mary Flaikfield, 76.
Metrical elegies, 140.
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M , Sir Robert, his reduced circumstances, 208.
Miners’ provisions, mode of obtaining from distant towns, 210, 211.
Mint in Scotland, 330.
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M , William, his ear nailed to the Tron for insolency, 23.
Mock Senator, a satire by Pennecuik, 473.
Money in Scotland at the Union, 330.
M , Robert, advertises for epitaphs, &c., for his Theater of Mortality, 382.
M of Skelmorley, plot of, 3.
M , Earl of, small debt-case, 77.
M ’ Account of Scotland, 269.
Mortality in Edinburgh (1743), 610.
M N , a Scottish serf living in 1820, 250.
M , Ensign, concerned in a murder at Leith, 48.
M , David, surgeon at Stirling, charge for drugs used by him to wounded of Killiecrankie, 47.
M of Foulis, his funeral, 560.
M , Donald, defends the Seaforth estates against government troops, 459, 468; his death, 471.
M , Elizabeth, her account of Scottish manners in eighteenth century, 571.
M of Caldwell’s journey from Edinburgh to Ross-shire, 406.
M , a tavern-keeper, in trouble on account of a false newsletter, 71, 144.
M , Clara, her violent letter to Lord Alexander Hay, 275.
M , Lady, of Stanhope, assault on, 478.
M , Sir Alexander, of Stanhope, his projects, 474; Strontian mines, 476; Ardnamurchan scheme, 474.
M , Nichol, murders his wife, 454; he is executed, 455.
Music, concerts of, in Edinburgh, 89, 139; rising taste for in Scotland, 432; Orpheus Caledonius, 434.
Musical instruments, curious advertisement of, 325.
Musselburgh, riding of marches at, 622.
N , a builder, at Inversnaid fort, 374.
Navigation of rivers, Henry Neville Payne’s petition, 217.
Negro slave, runaway, advertisement in Courant regarding, 453.
News, false, punishment for, 71.
—— -letters, 71; Murray, a tavern-keeper, sued for a false news-letter, ibid.
Newspapers, notices of early, 212, 313, 324, 414, 438.
N , Daniel, his case of adultery with Mrs Pringle, 60.
N , William, of High School of Edinburgh, anecdote of, 223.
N , Alexander, his System of Heraldry patronised, 276.
N , Earl of, troubled on return from France, 216.
Noblemen, imprisonments of, 68.
N , Dame Mary, petitions Privy Council in behalf of her children, 55.
Officers of the army, their accounts at hotels, 45.
O , Patrick, of Cairns, employed to guard the coasts against Irish importations, 243.
O of Forglen, his death and last injunctions, 533.
Orkney, a pirate taken in, 505.
O , Alexander, imprisoned, 14.
Painting in oil, early notices of in Scotland, 563.
Paper-manufacturing, 87.
Paragraphs from old newspapers, Appendix.
Paraphernalia of women, decided by Court of Session, 166.
Parochial schools, establishment of, in Scotland, 151.
P , Anthony, a quack medicine-vender, 261.
P , Archbishop of Glasgow, imprisoned, 12; permitted to live at certain places, 167.
P , William, promotes commerce and founds African Company, 121; his liberal ideas, 124; opposition to Bank of Scotland, 131.
Pates of Court of Session, 291.
P , Henry Neville, tortured and imprisoned for ten years, 39; proposes an improvement in river navigation, 218.
Pease-meal, nutritiousness of, 472.
Peebles, infanticide at, 19; prison not strong enough to secure a female culprit, 20; vested with a peculiar privilege, 51.
Perpetual motion, scheme of, by David Ross, 102.
P , ‘Duke’ of, his baptism, 383.
——, Earl of, taken prisoner at the Revolution, 11, 12; liberated, 66; again imprisoned, 67.
Perth, tumult at, on account of a picture, 565.
Peterhead as a harbour of refuge for vessels pursued by French privateers, 120.
Petrie’s Rules of Good Deportment, &c., 455.
Piper of Musselburgh, trepanned as a recruit, 44.
Pirates hanged at Leith, 458.
—— under Henry Evory seize a man-of-war, 150; a pirate in Orkney, 505.
P , Dr Archibald, introduces dissection in Edinburgh, 105; anecdotes concerning, 223;
brought before the Council for leasing-making, 224; raises an action for defamation against Rev. James Webster, 378; his death, 383; his writings, 384.
Pittenweem, treatment of witches there in 1704, 299.
Plantations, criminals and degraded persons transported to, without trial, 115, 211.
Planting first attempted in Scotland, 417.
P , Elias, murdered at Leith, 48.
Poor, vagrant, multitude of, 218; regulations for, proposed, 219.
Pope, the, tried and burned in effigy in Edinburgh, 3.
Porpoises thrown ashore at Cramond, 23.
P , Captain John, plays a match at golf with Hon. Alexander Elphinstone, 566; his unpopularity, 594; condemned for murder, 595; executed by the mob, 596.
Porteous riot, unpopular witnesses regarding, 600.
Post-office, general arrangements in 1689, 20; the post sometimes robbed and tampered with, 21, 74; post-boy robbed by Jacobite gentlemen, 32; act for establishing General Post-office, 125; violation of letters at Post-office, 265; affairs of, in 1710, 327, 357; improvements of, by Mr James Anderson, 400; accidents to postbags, 513; improvements of, 514.
Potato culture, 604.
Poverty of Scotland, traits of the extreme character of, 45.
Prayers, equivocating, 78; meetings for, 228.
Preaching in open air, 606.
Pregnancy, concealment of, act against, 26.
Presbyterian form of worship, innovation on, punished, 350.
Press, restrictions on the, 181.
Priests in trouble. See Catholics.
P of Clifton, fights a duel with Scott of Raeburn, 330.
Printing, art of, in Scotland (1712), 363.
Prisoners’ aliment, 208.
Prisoners detained, from inability to pay prison dues, 34.
Prisoners of Canongate Tolbooth, take possession of it, 71.
Prisons crammed with disaffected persons in 1689, 11.
Privy Council deals with Episcopal clergymen, 78.
Profaneness, proclamations against, 342.
Prussian grenadiers, recruiting for, in Edinburgh, 490.
P , John, pleads he is not a gentleman, 352.
Quack medicines vended, 260.
Quakers, persecuted at Glasgow, 57; persecuted at Edinburgh, 178; appear at Cross of Edinburgh, 467; build a meeting-house there, 621; one sets up a manufactory, 620.
Racing in Scotland, 454.
Raffle of Indian screens by Roderick Mackenzie, 310.
Railway, an early, at Prestonpans, 472.
R , Allan, Scottish poet, satirises metrical elegies, 140; his reference to Sir Richard Steele, 427, 429; reference to musical entertainments in Edinburgh, 432;
to the dancing assembly, 483; concern in theatrical entertainments, 518; lends plays, 544; erects a theatre, 598; his Gentle Shepherd acted, 624.
R , John, a poor man, imprisoned at the Revolution, 14.
Rebel prisoners removed from Edinburgh to Carlisle for trial, by virtue of ‘treason-law,’ 411.
Rebellion of 1715, 389; of 1745, 535.
Recruiting, unscrupulous system of, 43.
Recruits kept in jails, 79, 182, 601.
Regalia, controversy about its preservation, 264.
Reicudan Dhu, or Black Watch, 498.
Repentance Tower, subject of a rustic bon mot, 429.
‘Rerrick Spirit,’ strange story of the, 169.
Restoration of Charles II., celebrated by one Jackson, 371.
Restrictions regarding victual, troubles from, 210.
Revenue laws disrelished and resisted, 508, 589, 594.
Review of Highland Companies at Ruthven, 581.
Revolver, the, anticipated, 101.
R , Charles, a minister, in trouble about an irregular marriage, 190.
Roads made in the Highlands, 526, 561.
R R , first public reference to, 373; seizes Graham of Killearn, 420; is taken prisoner by the Duke of Montrose, but escapes, 421; forfeiture of his estate, 422; taken by Duke of Athole at Logierait, and escapes, 425; Rob’s bad excuse to General Wade, 500; his death, 624.
Robberies, great number of in 1693, 83; increase in Highlands from withdrawal of ‘Black Watch,’ 610.
R , Alexander, of Struan, 523.
—— ——, Duncan, dispossesses his mother, Lady Struan, of her property, 233.
R , the St Kilda Impostor, 179.
R , Lady, her charge against her husband, 143.
R , Lord, tries to repress cattle lifting, 31; prosecuted by his lady, 143.
R , Master of, killed, 117.
Rope-performers, Italian, 582.
—— -work established, 87.
R , Bishop of Edinburgh, his death, 452.
R , Earl of, pranks of, 604.
Ross-shire, election for, on a Saturday, 341.
R , Captain, raises sunk treasure, 551.
Royal Bank of Scotland, started, 537; rivalry of banks, 537.
Royal burghs, convention of, curious details concerning, 51.
R , Thomas, his connection with Dr Pitcairn, 385; improves the classical learning of Edinburgh, 438.
Rum, sale of forbidden, and subsequently permitted, 277.
R , Earl of, ‘bangstrie’ upon his property, 158.
Saddle, Elastic Pacing, invented, 101.
St Cecilia, feast of, celebrated in 1695, 139.
St Cecilia’s Day, celebrated in Edinburgh with a concert, 139.
St Kilda, account of, 168.
—— —— islanders acquire a minister, 178; curious peculiarity attending the inhabitants, 181.
St Luke, School of, institution of at Edinburgh, 564.
Salaries of judges of Justiciary and Court of Session, 303.
Salmon-fishery in Scotland (1709), 353.
Salt proposed to be made in a new manner, 154.
Salters and miners considered as slaves or necessary servants, 248.
S and M , Lords, seized by Master of Lovat, 185.
Sanctuary (Holyrood Abbey), taken advantage of by Patrick Haliburton, &c., 349.
S , Hon. Patrick, a boy, bewitched, 449.
S ’ engine for raising water, 237.
Scavengering of Edinburgh, 593.
Schools, parochial, establishment of, in Scotland, 151; plays acted at, 584.
Scots Magazine established, 603.
S of Raeburn killed in a duel, 330.
——, Walter, of Kelso, his marriage, and letter describing it, 39; funeral of his father-in-law at Glasgow, 387.
Scriptures, a multitude of copies of, distributed in the Highlands in 1690, 39.
S , Earl of, in rebellion of 1715, 391, 393; again in rebellion in 1719; his forfeited estates kept for his use by Donald Murchison, 459, 468; his ingratitude to Murchison, 471.
Secession, The, a schism in the kirk, 588, 625.
Second-sight, described by Martin, with instances, 278.
Servants, register-office for, proposed in 1700, 244.
Session, Court of, new judges appointed for, 10;
its purity under suspicion, 291; tyranny of, 293; severity of judges of, 371; salaries of judges, 303.
S , Hon. James, accused of robbing a post-boy, 32.
Settlement, an inharmonious, 580.
Sharps, a trial at designed, 209.
S , Christian, of Bargarran, her case, 167; thread spun by her, 510.
S , Sir John, of Greenock, his marriage, 240; kills Mr Houston, 402.
S ’ telescopes, 567.
S , Sir R., claims a share in Adair’s maps of Scotland, 42; his concern in originating a botanic garden, 81; his death, 619.
‘Siller,’ origin of term in Scotland, 212.
Silver-mine at Alva, 247.
S , Professor John, teaches Arminianism, 441.
Skye, Isle of, Second-sight in, 280.
Slaughters—town-clerk of Glasgow by Major Menzies, 103; Master of Rollo by Graham of Inchbrakie, 117; Houston, Writer to the Signet, by Kennedy of Auchtyfardel, 321; Cowpar of Lochblair by Ogilvie of Cluny, 322; Robert Oswald by Baird of Sauchtonhall, 322; by Master of Burleigh, 326; of Mrs Kincaid by her husband, 473; of Campbell of Lawers, 473; a boy Cairns killed, 547.
Slave (or ‘perpetual servant’), man adjudged to be for theft, and handed over to Sir John Areskine of Alva, 246.
Slave, negro, advertisement of a stolen one found, 453.
Slavery of salters and miners till 1775, 249.
