Bacillus Subtilis

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The Biological Resources of Model Organisms

Robert L. Jarret, Kevin McCluskey

The Bacillus Genetic Stock Center/ Bacillus subtilis

Publication details https://www.routledgehandbooks.com/doi/10.1201/9781315100999-3 Daniel R. Zeigler Published online on: 02 Aug 2019

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The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The publisher shall not be liable for an loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 References Conclusions The BacillusGeneticStockCenter Advantages of The Erasof Bacillus subtilis The Genus Introduction CONTENTS Abstract: Databases Use ofthe Collection Maintenance andDistribution Scope Mission Statement Establishment The “Recombinant The “Genetics Era” The “Classical Era” Geobacillus The The A Taxon withMany Dimensions A Taxonomic Explosion Its main collection now contains more than 11,000 more than collection now includes accessions that contains Its main 1970s. the in Stock Genetic Bacillus was Center use, initiated the widespread their to response In research. medical and agricultural, valuable industrial, in have cycle life them unique made characteristics other Their planet. and this every conceivable on have environment virtually isolated from bacteria, been The “Post-Genome Era” 3 Bacillus cereus Bacillus subtilis

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...... Bacillus Bacillus ...... 44 40 40 40 40 46 48 36 36 35 38 38 49 49 39 39 39 45 42 43 43 43 41 41 Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 INTRODUCTION 36 ing by binary fission. Generationtimes for many species may be asshort as ahalf ple nutritionalrequirements. Under idealconditions,they proliferaterapidly, divid allowed thesebacteriatosurvive andthrive onaglobalscale(Figure 3.1). many ofthemrequiringaremarkabledegree ofmulticellularcooperation,which have taxonomic trait. They are thecenterpieceofadiverse rangeofdevelopmental options, a muchlarger framework. Endosporesarefar morethanamorphologicalfeatureor whileaccurateforthe purposesoftaxonomy, needstobeplacedin This definition, these sporesarevery resistanttomany adverse conditions”(Logan andDe Vos 2015). and occasionallyaslongfilaments.Endosporesareformed, nomorethanonetoacell; “rod the definitionremainsessentiallysame: revolution ushered inbyrecenttechnologicalandtheoreticaladvances in destructive 1973).Morethanfourdecadeslater, agencies”(Gordonet al. despitethe endospores thataremoreresistantthanvegetative cellstoheat,drying,andother book, “encompassestherod-shapedbacteriacapableofaerobically formingrefractile “The genus GENUS THE will remainavailable inperpetuityformembersoftheresearchcommunity. distributes, andassemblesdataregarding thesemutantsandgenetictools,sothatthey Genetic StockCenter(BGSC)exists asasteward ofthislegacy. It collects, maintains, sincethegenomesequenceofstrain168was determined. The Bacillus the 20 years have beendeveloped of over thepast70 years important modelorganism. Thousands ofusefulgeneticmutantsandstrainlibraries subtilis comprises atleastthreebacterialfamilies anddozensofgenera.Onespecies( Modern sequence-basedtaxonomicmethodshave revealed that has practicalconsequences,many ofthempotentiallybeneficial,forhumanbeings. a highly successful adaptation but also (Zeigler and Nicholson 2017) and is not only developmental suitehasbeentermedtheBacillusLifestyle new populations. This tions areonceagain favorable forgrowth, sporesgerminateandgrow outtoestablish inert restingcellthatishighlyresistanttomostenvironmental insults. When condi high degree ofmulticellularity. Onespecializedtype,theendospore,isametabolically tions differentiate intosubpopulationsofdifferent celltypes,many ofthemshowing a growth, cellspropagate rapidly. When nutrient sourcesaredepleted, organisms thathave adopted a common lifestyle. When conditions are favorable for Bacillus sensulato and stored under conditions that maintain their long-term of viability. their Strains maintain conditions under that stored and 67 12 in species genera of Most isolatesofthegenus collection, on request. able the from Bacillus ‐ shaped, straightorslightlycurved, occurringsinglyandinpairs,somechains, ) andoneparticularlaboratorystrain( , sets of phages and plasmid tools, and associated resources are avail are resources of associated , sets plasmid tools, phages and and Bacillus

BACILLUS BACILLUS comprisesanenormousandphylogenetically diverse groupof ,” wrote Ruth Gordon and colleagues in their authoritative hand AND THE BACILLUS THE AND LIFESTYLE Bacillus Bacillus The Biological Resources of Model Organisms of Model Resources Biological The anditsclosestphylogenetic relatives have sim . Isolates can usually be easily propagated easily propagated be usually . Isolates can Bacillus B. subtilis B. subtilis bacteriahave cellsthatare research, especially during research,especiallyduring 168)have emerged asan Bacillus sensulato Bacillus popula Bacillus Bacillus biology,

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Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 resistant toa variety ofenvironmental insultsincludingUVradiation, abrasion, ery, andacondensedprotein-boundchromosome(Huang andHull2017). They are cell membrane,adehydrated cytoplasm with astartersetofgeneexpression machin an option of last resort—endospore formation. These living time capsules include a 2002, ment (Berkaet al. Yuksel 2016).Finally, et al. theBacillusLifestyleincludes machinery isassembledthatallows cellstobindandimportDNA from the environ “K-state”, a developmental stage in which growth and cell division are suppressed and Alternatively, killing factors, allowing somecells tocannibalizeothers(ShankandKolter 2011). cells secreteamatrixthatbindsthepopulationintobiofilm (Claessenet al.2014). acids forthebenefitofentirepopulation(Veening 2008a).Othersessile et al. potential nutritionalsourcesintheenvironment intosugars, nucleotides,andamino massive quantitiesofdegradative enzymesandantimicrobials,perhapsconverting for growth. The sessile chainsdifferentiate further, withonesubpopulationsecreting cellsmaybeabletolocate microenvironments thataremorefavorableThe motile motile singlecellsandsessilechainsquicklyappear(Mukherjee andKearns 2014). 2015, Veening 2008b).In et al. at leastpartofthepopulationsurvives theenvironmental challenge(Normanet al. of optionshasbeenseenasabet-hedgingstrategy, increasingthelikelihood that lations emerge, each pursuing a different developmental path (Figure 3.1). This suite Bacillus conditions approximatingtheidealoccuronlysporadically. When apopulationof hour orlessinthelaboratory(Zeigler, unpublishedobservations). In nature, however, of celltypes. conditions permit.Underunfavorable conditions,subpopulationsdifferentiate intoavariety FIGURE 3.1 The Bacillus Genetic Stock Center/ Stock Genetic Bacillus The Rather lessaltruistically, incertainspeciesthesematrix-builders mayalsosecrete experiences nutrientdepletion and entersstationary phase, several subpopu

The B. subtilis Bacillus anditsrelatives canformsubpopulationsthatenterintothe Lifestyle. B. subtilis Bacillus Bacillus subtilis Bacillus cultures,forexample, subpopulationsof mayproliferaterapidlywhenenvironmental 37 - - - Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 bacteria have attracted intense interest as a model system for studying developmental group oforganisms thathave adaptedacommonsetofsurvival strategies. These matter ofhours(MoirandCooper2015).Rapidproliferationbegins again. conditions areonceagain favorable, sporescangerminateandinitiateoutgrowth ina for longperiodsoftime,yearsorperhapscenturies.However, whenenvironmental remain metabolically inert desiccation, lysozyme, andorganic solvents. They can 38 It is beyond thescope ofthis(andperhapsany) review toadequately summarize allof have been isolatedfromnearlyevery conceivable environment fromaroundtheglobe. Isolates from a website (http://www.bacterio.net/-classifphyla.html#firmibacteria) (Parte 2014). the relevant pagesontheListofProkaryoteswithStanding inNomenclature(LPSN) rapidly, sotheinterestedreaderisencouragedtoaccessmorecurrentinformation on cation of Bacilliaceae in thefamily time of writing, there were four genera in the family At the clustered intoseveral distincttaxonomicfamilies besides theclassical actually required(Priest1993)toaccommodateknown diversity, andthatthesegenera tilis support thecreationofatleastfive genera,including Bacillus genus viously imagined. This revolution hadanespeciallydramaticimpactontheclassical primary Domainsonthetreeoflife—werefar morephylogenetically diverse thanpre superseded, itwas quicklyrealizedthatthebacteria—now elevated tooneofthethree et al gene(Fox based phylogenetic treebasedontheuniversally conserved 16SrRNA scientific revolutions ofthetwentiethcentury, thedevelopment ofaDNA sequence- genus the within species of handful the of scope bacteria, but limited focus to important on an It was born. BGSC which into the was paradigm the This was media. on discriminatory growth activity; and acid production; and enzymatic morphology; utilization carbohydrate age: colony,available DNA before Recombinant dawn of the the spore and cell, technologies designations. species Her classificationlimited the key use made of 1973), she was able every classify to available isolate then using her to only 18 Ruth completed Gordon handbook her When a affecting thepublichealthandeconomicdevelopment ofhuman society. biology. As describedbelow, they alsohave many currentandpotentialapplications

t t Over thenext decade,thereoccurredoneofthemostimportantandfar-reaching Bacillus anditsclosestrelatives. It was quicklyrealizedthatmany additional generawere axonomic axon . 1980, Woese andFox 1977). When conventional classificationsystemswere Bacillus species,they suggested that thehighdegree ofDNA sequence diversity would Bacillus sensulato

W , then,encompassesanenormous,phylogenetically diverse, andancient it alone. Those 74generacomprise many hundredsof species. The classifi Paenibacillaceae Bacillus sensu lato H . When Carol Ash andcolleaguesappliedthenew technologytoexisting

e m xplosion any

d Bacillus imensions —the oldgenus , 13inthefamily , each featuring some variant of the Bacillus Lifestyle . The Biological Resources of Model Organisms of Model Resources Biological The Bacillus Planococcaceae The Genus Bacillus Genus The ofGordon—continuestoevolve Bacillus sensustricto Alicyclobacillaceae , and57inthefamily (Gordon et al. al. (Gordon et Bacillaceae for B. sub , ten , ten - - - . Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 The Bacillus Genetic Stock Center/ Stock Genetic Bacillus The t review oftheseorganisms hasbeenpublishedelsewhere (ZeiglerandPerkins2015). and medicalapplications. They can onlybeintroducedbrieflyhere. A more thorough number ofspecieshave proven tobeespeciallyimportantforindustrial,agricultural, the phylogenetic andecologicaldiversity thatthey represent.However, amuchsmaller genus will require an expansion an of its genetic require toolkit. genus will 2015). al. exploitation Further of the using lignocellulosic et (Hussein feedstocks for platforms second-generation potential biofuel as attention production garnered 2016). (Huesca-Espitia et al. sterilization More recently, genus of members the have mophilus (Zeigler 2014). nature easily isolated from are and tribution have for elevated aworldwide requirement temperatures, despite their growth dis genus thermophilic of members the the of group are note A third g genes (Bravo for crops of transgenic insecticidal et al.sources 2011, Roh et al spraysThey have as formulated whether or as found wide application agriculture, in nematodes. and of including range insects invertebrates, pathogenic anarrow to are that toxins one or more proteinaceous make but instead vertebrates, or other humans most In contrast, et al aprotective capsule and (Friebe toxin lence due athree-component to anthracis 2016). et al. (Duport food to poisoning leading or emetic toxins diarrheal 2017). of fields array an applications in et al.(Ceuppens 2013, and Sanchis Patino-Navarrete The t and livestock (Elshaghabeeet al observations have raisedinterestintheuseofBSGisolatesasprobioticsforhumans Thailand, and Vietnam (Chenet al. 2012,Kanesakiet al. 2018,Kimet al. 2015). These mentation organisms fortraditionalricebranorsoybean-based foodsinKorea, Japan, rhizobacteria (Fan 2017, et al. Ye 2018).Stillothermembers oftheBSGarefer et al. its relatives have been shown to have significant potential as plant growth-promoting studying dispersalofanthraxspores(Sellaet al. 2015). dicator strainforthesterilization/decontaminationindustryandisasafesimulant atrophaeus tilis a dozencloselyrelatedspecies,containsseveral otherimportantmembers.Like components. The biofuel including theproductionofenzymes,vitaminsandothernutritionalsupplements, a key roleasaproduction platforminmany sustainablefermentationapplications, Practically usefultaxaareepitomizedbytheindustrialworkhorse, H H eobacillus e e ,

B B B. licheniformis Bacillus cereus Bacillus acillus acillus Bacillus cereus Bacillus spores are already the industry standard as a biological as for indicator steam standard industry the already are spores is the causative agent of the serious vertebrate disease anthrax, its viru anthrax, causative is the disease agent vertebrate serious of the , whichproducesablackpigmentonsuitablemedia,isanimportantbioin

su cereus B tilis B. thuringiensisB. whichisanindustriallyimportantproducerofenzymes. Group (BCG) Group includes significant with several species other

itself is an important food spoilage organism that can produce produce can food that spoilage organism important itself is an g

g roup Bacillus subtilis roup . 2017,Mingmongkolchai andPanbangred 2018). isolates have pathogenicity to no demonstrated Bacillus subtilis Bacillus Group (BSG), an informal grouping of about Group(BSG),aninformalgroupingofabout Bacillus amyloliquefaciens Geobacillus stearother Geobacillus Geobacillus B. subtilis . It plays . It plays Bacillus Bacillus Bacillus Bacillus . . which, which, 2007). 2016). 2016). B. sub and and 39 ------Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 Burkholder, chose ATCC 6051 Working inthe1870s,FerdinandCohn,abacteriologist atCornell(Geneva), allowed BACILLUS SUBTILIS taxon. of this importance the multidimensional applications, sufficient examples butdemonstrate to these are 40 could be genetically transformed by purified DNA (Spizizen 1958)usheredinthe could begeneticallytransformed bypurifiedDNA (Spizizen then at Case Western Reserve University. His subsequent discovery that strain 168 Several yearslater, asmallsetofthe Yale mutantswerepassedontoJohnSpizizen, t ATCC 6051 Bacillus became thenomenclaturaltypestrain,not only forthespeciesbut alsoforthegenus the University ofMarburg isolate astheclosestmatch(Conn1930). The Marburg lished descriptionwithacollectionoflaboratorystocks and selectedastrain from HaroldJ.ConncarefullycomparedF. Cohn’sisolate hadbeenlost.In 1930, pub 1946).FerdinandCohn’s original (Gordon andSmith1949,et al. ization todevelop ataxonomic systemtocategorize them,creatingorderfromchaos wide variety ofnaturalsources.However, thisrequiredtedious,methodicalcharacter Aerobic, endospore-formingbacteriacouldbeisolatedquicklyandeasilyfroma t OF THE ERAS were tofollow. Bacillus organism was thecausative agentforanthrax(Koch 1876),hefirmlyestablished Koch (thenaphysician working inPoland)showed thatamorphologicallysimilar film formation(ZeiglerandNicholson2017). WhenCohn’s contemporary, Robert by arangeofdevelopmental pathways includingmotility, sporeproduction,andbio opportunistic decompositionofbiomassuntilkey nutrientsweredepleted,followed the BacillusLifestyleasdescribedabove, thatis,aperiodofrobust growth fueledby (Cohn 1872).Bystudyingwhatwas probably a filmformedonthesurface oftheculture,whichgrew intoathick,flocculent pellicle that transitionedintostationaryfilamentsandthendeveloped endospores.Eventually a bacterialculturetomultiplyinboiledhayinfusions.He reported seeingmotilecells come (Zeigleret al.2008). called 168,was destinedtoplayalarge rolein (Burkholder andGiles1947).Oneoftheirmutants,atryptophan auxotrophthey ments designed to test the recently developed “One Gene One Enzyme” hypothesis NCIB 3610 H H e e Many other species of species Many other “ “ g c lassical enetics t was depositedinthe American Type CultureCollection(ATCC). It as as an important topic for microbiological research. Decades of research T T . In the late1940s,two Yale. In the microbiologists,NormanGilesandPaul andlaterintheBritishNationalCollectionofIndustrial Bacteriaas

e e BACILLUS ra ra ” ” , A MODEL ORGANISM Bacillus sensu lato sensu Bacillus BIOLOGY T asthesubjectofaseriesmutagenesisexperi The Biological Resources of Model Organisms of Model Resources Biological The could be singled out for their practical singled out could be practical for their Bacillus subtilis Bacillus researchinthedecadesto , Cohnhadobserved B. subtilis - - - -

Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 The Bacillus Genetic Stock Center/ Stock Genetic Bacillus The insights intothecomplexities oftheBacillus Lifestyle(Schaeffer 1967). This culmi ping. Someoftheseexperiments usedasporogenousmutants,providing increasing of studies employing mutagenesis, phenotypic characterization, and genetic map 1961). A picture ofthe opment. Soonbacteriophagetransductionwas addedasagenetictool(Takahashi to elucidatetheprocessesunderlying “Genetics Era”whenbiochemicalexploration was combinedwithgeneticanalysis ing in the organism (Liu et al. 2017). et al. (Liu organism the in ing 2016), et al. (Peters engineer metabolic possibility of have rational the and created 2017) forgene (Koo et al. gene every essential “knockdown” atunable library and 2012),et al. have for single-gene generated every knockout non-essential libraries dozens of under physiological of conditions (Nicolas avariety transcriptome in states organism’s have the of laboratories, by accomplished a consortia measured also ally analysisenabled of the it study of and also continued isolated genes or the proteins, facilitated sequence amajor in milestone This was for completion. was sequence released. In November 1989, complete the annotated eight years required that nology it available was time, amassive atthe undertaking complete the genome Given for sequence organism. tech the the toward determining of consortium international an subtilis B. SangerAs DNA sequencing less expensive became more widely and available, cloned t developmentand of function, providedsophistication, they ever-deepening structure, the insights into 1983). fusions (Youngman in and grew ers et al. DNA techniques recombinant As to transposons Losickism and (Zuber 1983). could deliver that vectors were other constructed Still gene expression genes, organ facilitating the in fusionsgenerate studies reporter to out mutagenesis 1980). (Haldenwang et al. vectors were developed Other could that or knock subjected to cloned aselective with mapped genes tagged and be to marker development was the A major vector, integration of breakthrough the which allowed tilis circle replicons ofrolling 1978, Losick Sakaguchi and 1978, 1977). Segall and Ehrlich Nagahari The small, 1977, 1978, et al. Duncan of (Chi out cloning et al. organism of genesand the in The “Recombinant DNA Era” of t (Lepesant-Kejzlarovà et al.1975). nated withthepublicationofanun-gapped circular geneticmapfor H H e e The ensuing two decades can be termed the “Post-Genome Era.” The genome “Post-Genome the Era.” The genome termed be can two decades The ensuing , forming the basis of the first generation basis first ofof the (Ehrlich the cloning 1977)., forming vectors “ “ r p ost ecombinant genes of interest began to be sequenced routinely. In September 1989, routinely. sequenced genes be to of began interest In September 1989, - g enome B. subtilis B.

B. subtilis B.

dna e ra B. subtilis B. subtilis B. ” Staphylococcus aureus Staphylococcus , allowing saturation mutagenesis selectable with , allowing saturation mark

e ra cells. B. subtilis B. ” B. subtilis B. Bacillus subtilis Bacillus genomegraduallybegan toemerge fromhundreds as a biological as system. Ongoing gener efforts, Bacillus subtilis Bacillus Bacillus studies (Kunst et al. 1997). et al. (Kunst studies geneticists systematically working began physiology, metabolism,anddevel research began with the first reports reports first the with began research were found in function to B. subtilis B. sub B. 168 41 ------

Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 ADVANTAGES OF present generation. the to tunities oppor fresh (1997—present)—has and Genome Era alegacy of strains bequeathed (1958–1976), Era Genetics (1977–1996), DNA Era Recombinant the Post- the and 42 have atleastfourqualificationsallofwhich recently argued thatforanorganism tobeconsideredamodernmodel system, itmust and completelyinnocuous(Schallmey et al. 2004).LiuandDeutschbauer(2018)have relatives. easilygrown It is andmaintained,geneticallytractablenon-pathogenic B. subtilis historical survey above demonstrates,themostimportantstrainforthispurposeis Gram-positive phylum Firmicutes—thatmodelorganism is group ofbacteriawithhigheconomic,environmental, andmedicalimportance—the studyofanenormous the researchcommunity”(FieldsandJohnston2005).For the ground fordeveloping new technologies,whichtypicallyspreadquicklythroughout experiments to illuminate” obscure biological processes and can serve as a “proving many dedicatedscientists, thatthey cannow “be drawn upon forformulatingincisive Model organisms arethosethathave beenstudiedsofrequently, forsolong,andby Each of these eras in in eras ofEach these When working with the the with working When 2. 3. 1.

ment algorithms that essentially import annotations from other organisms. organisms. other from annotations import essentially that ment algorithms align and using searching sequence pipeline ofuse agenome annotation Most genome gene annotations. make projects data-driven Robust, curated, ordered knockout collectionsderived fromit,areavailable fromtheBGSC. available. Many ofthesetools,inadditiontothemodelorganism itselfand epitope tagging,marker genefusion,andchromosomalintegration arereadily of multipurposeplasmidvectors designedforcloning,regulated expression, transduction (Valero-Rello et al. 2017, Yasbin and Young 1974). A large variety 2012)andbacteriophage SPP1-mediated troporation (Meddeb-Mouelhiet al. Natural competencecanbesupplementedwithothertools,most notablyelec 2002). thechromosome(Berkaet al. enzymes forintegrating thisDNA into tion with exogenous DNA, accompanied by an activation of recombination the “K-state”duringwhichcellsbecomecompetentfornatural transforma one componentoftheBacillusLifestyleisdevelopmental processtermed ofgenetictools formanipulationoftheorganism. For A suite 2016).et al. For (Mars and studied identified have similarly RNAs been Regulatory also 2012). al. 2015, al. Nicolas et et of conditions (Arrieta-Ortiz a variety under haveand studied identified been Components transcriptome of the 2009). et al. the (Barbe genomeof nologies,sequence accuracy the refined of use next generation full tech sequencing making effort, resequencing 1997). recent over ago A more et al. twenty years (Kunst was determined above, discussed As ers. complete the genome of sequence promot and of products list genes, along their with inventoriedAn parts 168. This organism hasmany advantages 168. overThis organism mostofitsGram-positive B. subtilis B. BACILLUS SUBTILIS B. subtilis B. B. subtilis B. 168, then, the parts list is completely list 168, known. parts the then, The Biological Resources of Model Organisms of Model Resources Biological The research—the Classical Era (1930–1957), Era Classical research—the the system, researchers have system, to: researchers access B. subtilis AS A MODEL AS ORGANISM 168very clearlypossesses. Bacillus subtilis B. subtilis B. B. subtilis 168, 168, . As the the . As 168 168 ------Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3

vious generations andtheexciting new toolsthatcontinue tobecreatedinourday. munities asthesteward oftherichlegacy ofstrainsthathave beenproduced bypre throughout theworld.” servesThe BGSC thescientificresearchandeducationcom to distribute these materials without prejudice to qualified scientists and educators cloning vectors, andbacteriophageforthegenus goal ofthe BGSC isto“maintain genetically characterized strains, The primarily m support fromtheNationalScienceFoundation sinceitsinception. staff hasreceived in1985,assumedthepositionofDirector. generous The BGSC DanielZeigler,chose DeantodirecttheBGSC.In 1997, whofirstjoinedtheBGSC firms interestedinthefermentationbiologyandgenetics of Laboratories) andCharles A. Claridge(Bristol Laboratories)torepresentindustrial sisted oftheoriginalgroupacademicscientists,joinedby RobertErickson(Miles committee, chaired by Copeland, con of funding for the culture collection. This 6–9, 1975atCornellUniversity, formedanorganizing committee toexplore sources to interestedpersons.Participants attheFirstConferenceon key species,documentthestabilityandvalidity ofthesecultures,anddistribute them need foracentralizedorganization tocollectgeneticallycharacterizedstrainsfrom Arnold Demain,JamesCopeland,HarlynHalvorson, andDonaldDean, perceived the and medical research. Several geneticists, including Frank Young, Manley Mandel, cies fromthegenus full fruition, and hundreds of well-characterized mutants were available. Other spe Society forMicrobiology. Era” of The “Genetics tracesitsoriginstothe 1974 and1975annualmeetingsofthe The BGSC American e THE BACILLUS GENETIC STOCK CENTER The Bacillus Genetic Stock Center/ Stock Genetic Bacillus The stablis ission 4.

responsible for old errors percolating through a database (Gilks et al. (Gilks 2002). adatabase responsible through for percolating old errors is sometimes and rapid, is error proneto although annotation, Machine Josas, France. National delaRecherche Agronomique (INRA)researchcenteratJouy-en- 2008), andthe the GenoList platform for genome searching and comparison (Lechat et al. 2018), including theBsubCycdatabaseofmetabolicpathways (Caspiet al. outlinks, SubtiWiki 2.0 serves asacentralhubforcomplementaryplatforms, tory pathways, andgeneexpression foreachlocusinthegenome. Through porates andgraphicallypresentsdataonprotein-proteininteractions,regula alsoincor above, ismuchmorethananalternative annotationplatform.It Computational platformsforsystems-level analysis.SubtiWiki 2.0,mentioned 2016). et al. available is also for (Michna organism, the pedia 2018). et al. (Borriss genome encyclo curated 2.0, acommunity SubtiWiki on published data based are annotations and years, for overcurated 20 of sequence The genome H

s ment tatement Bacillus B. subtilis werealreadyproving useful inindustrial,agricultural, ExpressionDataBrowser maintainedbytheInstitut B. subtilis B. Bacillus subtilis Bacillus 168, in contrast, has been manually manually 168, been has contrast, in Bacillus B. subtilis andrelatedorganisms and Bacillus research was comingto Bacillus . The committee , held August , - - - 43 - - - - Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 Zahler (Cornell), Ernst Freese (National Institutes of Health), Reilly (Case Institutes (Cornell), (National Freese Bernard Zahler Ernst scientists including Stanley retired collections from strain a select of group personal focus news and catalogs special blogs various in site. on the contains The warehouse BGSC the website from searchable is fully (http://www.bgsc.org) is publicized and collection warehouse. The main astrain collection and The BGSC amain comprises s 44 B. atrophaeus B. pumilus B. amyloliquefaciens B. licheniformis B. megaterium B. cereus B. thuringiensis Other Gene knockdown Gene knockout Bacillus subtilis Classification Stock Center Collection BacillusMain Genetic the in of Components Number and Classification 3.1 TABLE antibiotic producers and plant-associated microbes, bacteria, marine philes, extremo with own right, their in interesting are groups taxonomic The smaller control ofatunablepromoter(Peterset al. 2016).Otherwell-representedgroupsare: BEC knockdown library, in which every essential gene has been placed under the erythromycin orkanamycinresistancecassettes,respectively (Koo 2017),andthe knockout libraries,inwhichevery non-essentialgeneisindividually inactivated with B. subtilis Over 80 in 12 genera of (Table 3.1), an increase of over 400 available are on request. strains Individual public the database. in mented not docu but are they interest, historical of their because maintained lections are Western University and (Stanford). of Joshua Minnesota), and col Lederberg These cope • • • • 2017, the main collection was comprised of 11,498 accessions As of July

B. subtilis Lysinibacillus sphaericus Geobacillus methods, megaterium B. cluster,species pathogen The insect speciescluster % speciescluster 168. Among themarethreesystems-biologylibraries:theBKEand BKK oftheaccessionsarederived fromtheGram-positive modelorganism, 168mutants isolates cluster Bacillus sensu lato , a group of industrially important obligate thermophiles, and obligate thermophiles, important of, agroup industrially , a species with large cells useful for direct visualization visualization for useful cells direct large with , a species B. thuringiensisB. Number , a species pathogenic blackflies. mosquitos to , aspecies and 7935 9596 244 108 198 314 10 23 43 80 9 The Biological Resources of Model Organisms of Model Resources Biological The , along with sets of phages and plasmid tools. % since July 2013. Represented are 67 species and other members of the of members the other and Bacillus Plasmid tools Other Ureibacillus Sporosarcina Rummelibacillus Paenibacillus Lysinibacillus Geobacillus Brevibacillus Aneurinibacillus Bacillus Classification phagesandlysogens sp. sp. sp. sp sp. sp.

sensu lato sp. sp. B. cereus B. Number 741 155 161 40 47 15 18 3 1 4 2

- - - Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 set for surface displayset for on of surface proteins for biology synthetic of parts et al. (Popp 2017, et al. Radeck 2013); “Sporobeads” the such700 tools available. BioBrick “Bacillus the Included are Box” 1.0 2.0 sets and for manipulating isolates, have publicly available genome sequences. collection, most type of wild the them in Currently, overrepresented. strains 200 for long term maintenance. After liquid cultures have cultures liquid sporulation, undergone bulk After for maintenance. long term cereus of 2xSG(Zeigler, unpublishedresults).Othersporulationmediaarepreferable for more commonlyusedin medium (abbreviated SSMor lessaccuratelyDSM)(Schaeffer et al used attheBGSC,is2xSG(LeightonandDoi1971).Schaeffer’s complex sporulation of spores. A very effective sporulationmedium for Bacillus sensulato Base (withoutblood),althoughsomeprefer Trypticase Soy Agar. For many isolatesof Most and shouldbepropagated athighertemperatures;theBGSCroutinelyuses50 sensu lato than doesLB(Zeigler, unpublishedresults).Isolatesfromotherspeciesof for higheryields,healthierstationaryphasecells,and sporulationfrequencies tously in suggests thatmany labs useLysogeny Broth (LB), thegrowth mediumfoundubiqui these species. Anecdotal evidence, togetherwithaperusalofthepublishedliterature, adequate. The BGSC typicallyusesNutrientBrothNo. 2 (NB;Oxoid)forpropagating under aerobicconditions.Mostgeneral-purposecomplex microbiologicalmediaare and theirclosestrelatives, grow rapidlyatmesophilictemperatures(30 Level 2. Some of members organisms. the ity, including all analysis. Very few of members high-throughput and manipulation robotic save to further both facilitate to and space 96-well or compatible in microplates microvials, tendency libraries store to larger increasing the ago innovation (Sanderson been Zeigler has 1991). and main The two nearly decades detail in were that described methods the motivation modify to easily, very stored and gated excellent with long-term little viability. been There has Lifestyle, Bacillus of aconsequence As their m in replicate vector collection are able gene expression (Guiziou toolkit et al. 2016); more. many Most and BGSC of the et al. 2017); vectors (Radeck integration a toolbox “personalized” for atun creating The Bacillus Genetic Stock Center/ Stock Genetic Bacillus The aintenance For any Members oftheindustriallyimportantgenus Isolates fromthemostcommonlystudiedspecies,including genetic cloning other tools vectors and distributes and maintains The BGSC also Geobacillus anditsrelatives orforthebioindicatorstrain Bacillus anthracis Bacillus Escherichia coli maypreferothermediaandrequiredifferent growth conditions. Bacillus

and B. subtilis B. isolatesintheBGSCcollectiongrow wellon Tryptose Blood Agar B. subtilis B. , incubationfor3–4 days inNBissufficienttoproduceagoodyield

isolate capable of producing them, spores are the preferred form form preferred the isolate capable are spores of them, producing d istribution B. subtilis labsandmolecularbiologyprotocols.However, NBallows cultures are not stocked at the BGSC. not stocked atthe are cultures isolates, can be treated as innocuous Biosafety innocuous as Level 1 treated be isolates, can and other important species. Currently there are over are there Currently species. important other and Bacillus sensu lato sensu Bacillus Escherichia coli Escherichia labs,althoughitssporeyields arelower thanthose B. cereus Bacillus subtilis Bacillus B. subtilis B. group should be treated as Biosafety as should treated group be Bacillus Geobacillus B. subtilis and are distributed in that form. that in distributed are and spore coats (Bartels et al. 2018); et al. (Bartels coats spore B. atrophaeus are pathogenic; major large are the isolates can usually be propa be usually isolates can anditsrelatives, routinely are obligate thermophiles areobligate thermophiles B. subtilis (Buhret al . 1965) is perhaps 1965)isperhaps , ° B. cereus C–37 . 2008). Bacillus Bacillus ° ° C) C) 45 C. C. B. B. - - - - , Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 should be harvested during the exponential phase of growth. The cryovials can be be can The cryovials of exponential phase growth. the during should harvested be of mutants asporogenous conditions and laboratory standard under do not sporulate isolates that 10 asterile in directly suspended microbiological plate loop a sterile with and agar of a sporulation surface the from scraped be cryovials. to Alternatively, can cultures pension transferred sporulated concentration of afinal to glycerol10 added be sterile can 46 out as especially popular (Table 3.2). The most commonly requested stock, by stock, a mostrequested commonly 3.2). (Table popular The out especially as five-year past the However,period. once during be singled accessions can certain valuable partinthescientific infrastructurebyservingasatoolboxforinnovation. inventions based in partonBGSCstrains.In short, theBGSChasplayedameasurably During thissameperiod,there have alsobeenatleast69USpatents issueddisclosing in arsenicbioremediation,andthedevelopment of investigation of clarity, someofthesmallerresearch fronts areexciting, fast moving fields,suchas the greatest use of BGSC strains in published papers. Although omitted from the figure for 3.2depictsthosefrontswiththe into 32researchfrontsinBGSCanalyses.Figure broad impactonavariety ofimportantfields. These publicationshave beengrouped original sourceisonlycitedintheinitialreference.Even anincompletetallyreveals a estimate asfrequently, ifaseriesofpublicationsmakes use ofasetstrains,their acknowledged theBGSCasasourceofresearchmaterials. This is likely alarge under strains usedinteachinglaboratories.Since atleast522publicationshave April 2013, tion’s citationinpeer-reviewed publications.However, thismetricfails toaccountfor scientists andeducatorsin57nations.OnemeasureoftheBGSC’s impactisthecollec researchers whomake useofit.Duringthelastfive years,culturesweredistributed to breadthofthetaxon The u freeze-dried lyophiles,althoughtheBGSCdoesnot make useofthismethod. slants orinsmallPetridishes. Alternatively, asporogenousmutantsmaybetransportedin (Zeigler, unpublished results). These mutants may be shipped as cultures growing on agar paper undernormalambientconditions,withhalf-lives ontheorderofonedayat22 Earlyblocked sporulationmutantsdiequicklyonfilter cultures isnot recommended. spores willlastatleastseveral weeks,ifnot longer. Refrigerationofdisksor the diskstransferredtoasuitablegrowth medium.Undertypicalambientconditions, a business envelope. When they arrive attheirdestination,thepackets canbeopenedand sterile aluminumfoilpackets orinplasticwrap. The packets aremailedorshippedinside arethenwrappedeitherin spores canadsorbintothepaperasicemelts. The disks The frozen spore suspension is transferred to a small stack of filter paperdisks so thatthe inexpensive. A loopful ofspore-ladenicecanbescrapedfromthesurface ofafrozenvial. vive indefinitely conditions. these the (at underBGSC) at least decades for protocols. for sur cooling suspensions withoutphase, Spore any need will specific −80 mechanical in them bystored freezing se Well over half of the strains in the BGSC atleastWell the collection have in distributed over been strains of the half If stockshave beenstoredasfrozensporesuspensions,theirdistribution issimpleand

t H e

B. subtilis B. c ollection B. thuringiensis can also be stored in glycerol in stored be also solutions, can cultures but these Bacillus sensulato toxinsthattarget cancercells,theuseof % glycerol vials. to solution transferred and The Biological Resources of Model Organisms of Model Resources Biological The ° C freezers or in liquid nitrogen liquid vapor or in C freezers isseeninthediverse community of Bacillus % sporesasoralvaccines. (v/v) sus spore the and B. subtilis Bacillus Bacillus ° C - - - -

Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 a Strain 2012–June 30, 2017) (Cumulative, Plasmids BGSC and Strains July 1, Distributed Frequently Most 3.2 TABLE front. research identified an to belonging of references proportion the 2013 2018. indicates April March to from chart Pie strains 3.2 FIGURE 3A1 1A976 1A1 3A36 1A96 1A751 25A2 9A5 7A16 4Q7 1P7 4AA1 1A1133 4D4 4D1 3A38 10A6 1A747 The Bacillus Genetic Stock Center/ Stock Genetic Bacillus The

Bt, T abbreviation for Bacillus subtilis Bacillus subtilis Bacillus subtilis Bacillus subtilis Bacillus subtilis Paenibacillus Geobacillus Bacillus megaterium Bt israelensis Bacteriophage SPP1 Bt morrisoni Bacillus subtilis Bt kurstaki Bt kurstaki Bacillus subtilis Bacillus velezensis Bacillus subtilis Bacillus subtilis

polymyxa (See color insert.) (See Species B. thuringiensis. sp. a References citing use of Bacillus Genetic Stock Center Stock Center Genetic of use Bacillus References citing Total 265 85 60 74 76 30 30 30 31 33 36 36 36 40 44 45 45 55 Bacillus subtilis Bacillus pMUTIN4 pDR244 pNW33N pAX01 pMutin-GFP P pLIKE-int pDG1730 pBS3C-lux pBGSC6 pBS2E pLIKE-rep pA-spac pDG1662 P pSG1154 pBS4S pSG1156 liaG veg Plasmid + Conditional knockout Cre-production Constitutive expression Inducible expression Ectopic integration Expression reporter Simple integration Ectopic integration Inducible expression Inducible expression Ectopic integration Constitutive expression Fluorescent tagging Simple integration Fluorescent tagging Thermophilic cloning Inducible expression Fluorescent tagging Type Total 78 89 38 40 40 45 45 49 49 50 50 52 53 55 59 67 68 73 47 Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 fluorescent protein fusionfluorescent protein vectors. ducing bacteriophage SPP1 of expression avariety (BGSC and 1P7) vectors and andas serve to include fied trans geneticcloning hosts.tools the vectors Popular thermophilic and 4Q7) and have that lates characteristics; plant growth-promoting sion 1A1). parent, type Its wild classic the model organism, remains margin, large 48 base isupdated immediatelywhenever anew strainorplasmidisaccessioned into straindata are outputtedtoaformletter accompanying theshipment. The public in thestraindatabasefor requestedstocks,withtheadditionofa“notes”field, the contactinformationdisplayed onthewebsite. When ordersarefilled,alldata and theuserdatabase.Orders arealsoacceptedbye-mail,telephone,orfax, using mentation purposesandfortransfer ofdatatotheprivate strainusagespreadsheet erates adocumentthatisautomaticallyemailedtotheBGSC directorfordocu can beplaceddirectlyonthewebsitewithaconvenient onlineform;thisformgen who haspublishedonthestrain,oraphraseintitleof akey reference.Orders that mightexist initsrecord,forexample aspeciesname,mutantallele,anauthor sion for numbers genomic or 16S rRNA gene sequences. now also acces and includes media, key growth published references, recommended history, genotypic description), and strain codes, but or class, product tity original includes for key stock each (BGSC information accession number, iden taxonomic still BGSC at the website. engines search power to is used The database online the which language, SQL ANSI-compliant programming and ISO- the to changed since long has (Sanderson database Zeiglermunity 1991). and strain of the The format the of in users was thousands physically to that distributed package available a“catalog generate to mercially on diskette” relational database for records acom newer into accessions, weretogether similar with incorporated in catalog 1980.editionthe BGSCof first By data, strain the generate to these 1990, for everycollection. phenotypes provenance, It was item the and used in genotypes, names, accession strain computer, numbers, which linked on amainframe housed database, a proprietary generated effort 1970s,late a major programming in-house BGSC. atthe In the long a priority has accession been data ofDigitization strain d Bacillus velezensis Bacillus ing includ requests, have species popular other been also certain from strains Standard have to engineered xylose-inducible 2011). Zhang and genetic (Zhang competence duction of foreign (Zeigler, proteins unpublished). for feature pro important an seven proteases, all secreted knockouts in with strain KO7 (BGSC 1A1133), developed 2016 in BGSC, at the is a marker-free, prototrophic quently were two requested developed more recently community. fre Also research the to (BGSCJH642 1A96) useful be to continue Other demand. high atabases The online search engine allows the user to locate a strain by any word or phrase B. thuringiensisB. (BGSC 10A6) and isolates that are toxic (BGSC 4D1, pests lepidopteran to are isolates that 4D4); B. subtilis B. Geobacillus laboratory strains, such PY79 as (BGSC 1A747) strains, laboratory and B. subtilis B. The Biological Resources of Model Organisms of Model Resources Biological The (BGSC 9A5) derivatives have that modi been Paenibacillus polymyxa NCIB 3610 NCIB Bacillus subtilis Bacillus B. subtilis B. B. subtilis B. T (BGSC 3A1 (BGSC B. thuringiensisB. Bacillus 168 (BGSC acces (BGSC 25A2) (BGSC iso derivatives. Strain SCK6 is a strain SCK6 is astrain genetics com genetics T ), is also in ), in is also (BGSC (BGSC ------Downloaded By: 10.3.98.104 At: 04:17 24 Sep 2021; For: 9781315100999, chapter3, 10.1201/9781315100999-3 Bravo, A., S. Likitvivatanavong, S.S. Gill and M. Soberon. 2011. M. Soberon. Bravo, and S.S. A., Gill S. Likitvivatanavong, et al. 2018. Harwood. C.R. R., Danchin, A. Borriss, Buhr, T.L.,Buhr, D.C. B.W. and McPherson of broth-cultured Analysis 2008. Gutting. Ceuppens, S., N. Boon and M. Uyttendaele. 2013. S., M. Uyttendaele. N. and Ceuppens, Boon Diversity of path of metabolic 2018. database et al. Fulcher C.A. The MetaCyc R., Billington, R. Caspi, P.R.Burkholder, 1947. in N.H. Giles. and mutations biochemical Induced of the analysis Microarray 2002. al. et M. Albano. R.M., J.Berka, Hahn, Bartels, J., S. Lopez Castellanos, J. Radeck and T. and J. Radeck Mascher. J., 2018. Castellanos, S. 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