Supplemental Material Vos and Didelot ‘A comparison of homologous recombination
rates in bacteria and archaea’
A. Supplemental Data for Table 1
B. Excluded Datasets
C. References
A. Supplemental Data for Table 1
Bacillus spp.
Strains of three species (B. cereus, B. thuringiensis and B. weihenstephanensis) isolated from
a forest near Versailles, France (Sorokin et al., 2006). Six loci were sequenced (clpC, dinB,
gdpD, panC, purF and yhfL). Strains not isolated from the forest site were excluded. All three
species live in soil. B. thuringiensis is an insect pathogen. B. cereus and B. thuringiensis can
be opportunistic pathogens, B. weihenstephanensis is not associated with disease.
A UK population of phylloplane B. thuringiensis was re-analyzed and found to have an r/m
value of 2.0 (CI 1.2 – 3.1) (Bizarri et al., 2008). Seven loci were sequenced (glp, gmk, ilv, pta,
pur, pyc and tpi) in 17 isolates.
Bartonella henselae
This Bartonella species is mainly associated with felines and can cause Cat Scratch Disease
as well as other complications in humans. Isolates form felines and humans from a wide
geographical range (Arvand et al., 2007). Seven loci sequenced (batR, gltA, ftsZ, groEL,
nlpD, ribC, rpoD).
Bordetella pertussis
1
Causative agent of whooping cough (pertussis) in humans. Worldwide clinical isolates, seven
loci sequenced (adk, fumC, glyA, tyrB, icd, pepA and pgm) (Diavatopoulos et al., 2005).
Brachyspira sp.
Anaerobic intestinal spirochaetes recovered from pigs, dogs, birds and a mouse in seven
European countries, USA and Canada. Species classification difficult. Seven loci used (adh,
pgm, est, glp, gdh, thi, alp); no tests for recombination in original paper (Rasback et al.,
2007).
Campylobacter insulaenigrae
Isolated from young, stranded northern elephant seals in California (Stoddard et al., 2007).
Seven loci sequenced (aspA, atpA, glnA, glyA, pgi, pgm and tkt).
Campylobacter jejuni
British isolates from a variety of sources downloaded from pubmlst.org. Seven loci sequenced
(aspA, glnA, gltA, glyA, pgm, tkt and uncA).
Chlamydia trachomatis
A small set of clinical isolates isolated from urogenital and eye (trachoma) infections
(Pannekoek et al., 2008). Seven loci sequenced (gatA, oppA, hflX, gidA, enoA, hemN and
fumC).
Clostridium difficile
Worldwide isolates from humans and several animal species (Lemee et al., 2004). Six loci
analyzed (aroE, dutA, gmk, soda, recA and tpi). Not all alleles were available for a seventh
locus ddl.
Enterococcus faecalis
2
Clinical isolates, only those STs present in Spain were included; seven loci sequenced (gdh,
gyd, pstS, gki, aroE, xpt and yqiL) (Ruiz-Garbajosa et al., 2006).
Enterococcus faecium
Dutch isolates from poultry and humans all belonging to AFLP genogroup B (Homan et al.,
2002). Seven loci sequenced (adk, atpA, ddt, gyd, gdh, purK and pstS).
Escherichia coli
Isolates from sand and water in the wave-wash zone of six sites along Lake Huron and the St.
Claire River in Michigan, USA (Walk et al., 2007). Seven loci sequenced (adk, fumC, gyrB,
icd, mdh, purA and recA).
Flavobacterium psychrophilum
Worldwide collection of fish pathogen samples (from different host species). Seven genes
sequenced (atpA, dnaK, fumC, gyrB, murG, trpB and tuf) (Nicolas et al., 2008).
Haemophilus influenzae
The first 50 ST’s in the www.mlst.net database (Meats et al., 2003). Effect of population
structure unlikely as many ST’s occur globally. Seven loci sequenced (adk, atpG, frdB, fucK,
mdh, pgi and recA). The dataset consists of different capsule types as well as some
unencapsulated isolates. Non-encapsulated strains rarely cause infection whereas capsulated
strains are a significant source of disease. It has been suggested that the former may
recombine more frequently than the latter (Meats et al., 2003; Perez-Losada et al., 2006); this
observation would be expected when disease-associated strains have epidemic population
structure.
Haemophilus parasuis
3
Two datasets were analyzed. One cluster of 79 mainly non-pathogenic isolates (Table 1) and a
cluster of 27 mainly pathogenic isolates (Olvera et al., 2006). An r/m value of 5.5 (CI 2.6 –
32.7) was found for the latter group. No information was available on capsule production.
Seven loci sequenced (atpD, infB, mdh, rpoB, 6pgd, g3pd and frdB). No congruence of
individual gene trees in original publication (Olvera et al., 2006).
Halorubrum sp.
Isolates from different salterns at Santa Pola near Alicante, Spain. Four loci sequenced (atpB,
ef-2, radA and secY). Original paper reports linkage equilibrium on the basis of the Index of
Association test (Papke et al., 2004).
Helicobacter pylori
European isolates from pubmlst.org. Seven loci sequenced (atpA, efp, mutY, ppa, trpC, ureI
and yphC).
Klebsiella pneumophila
Clinical (nosocomial) isolates from around Europe (Diancourt et al., 2005). Seven loci
sequenced (rpoB, gapA, mdh, pgi, phoE, infB and tonB).
Lactobacillus casei
Isolates classified as L. casei and L.paracasei (which cluster together), mostly from (diary)
food products from France (Diancourt et al., 2007). Also found in the human intestinal tract;
exact natural habitat unclear. Seven loci were sequenced (fusA, ileS, lepA, leuS, pyrG, recA,
recG).
Legionella pneumophila
Isolates from a local area around Valencia, Spain experiencing regular outbreaks (Coscolla
and Gonzalez-Candelas, 2007). Fourteen sequence fragments available, but many consist of
4
very short housekeeping gene fragments and longer intergenic spacer regions. Therefore, only
two gene fragments, asd and mip, were used. Low recombination rate in accordance with a
study on a large collection of global isolates (Edwards et al., 2008).
Leptospira interrogans
Clinical (leptospirosis) and rodent isolates from Thailand (Thaipadungpanit et al., 2007).
Seven loci sequenced (pntA, sucA, pfkB, tpiA, mreA, glmU and fadD).
Listeria monocytogenes
Spanish isolates from food and animal and human clinical sources (Salcedo et al., 2003).
Seven loci sequenced (abcZ, bglA, cat, dapE, dat, ldh and ldkA).
Mastigocladus laminosus
Isolate collected worldwide from alkaline hotsprings (Miller et al., 2007). Four loci
sequenced (argS, nifH, devH and narB). For the last three loci, only parts of the available
sequences were used due to large gaps.
Microcoleus chthonoplastes
Isolates from two mud flat populations in the North Sea and one population in the Baltic Sea
(Lodders et al., 2005). Two loci were used (KaiC and PetB/D); the available intergenic spacer
sequence was not used.
Microcystis aeruginosa
Isolates from Japan and mainland East-Asia as well as one British and one Canadian isolate.
All five Microcystis morphospecies present. Seven loci were used (ftsZ, glnA, gltX, gyrB, pgi,
recA and tpi). Evidence for recombination found in original paper using the SH-test but not
the Index of Association test (Tanabe et al., 2007).
5
Moraxella catarrhalis
The first 50 STs from the http://web.mpiib-berlin.mpg.de/mlst database that occur in Europe.
Seven loci sequenced (abcZ, adk, efp, fumC, glyBETA, mutY, ppa and trpE). The finding of
high HRR contrasts with a previous study (Perez-Losada et al., 2006) that utilized coalescent
methods on the whole Berlin dataset. This could potentially be due to inclusion of
geographically isolated groups between which no recombination occurs.
Mycoplasma hyopneumoniae
Can cause enzootic pneumoniae in swine. Most strains from Switzerland; several very closely
related strains from other countries included as well (four outgroup STs omitted) (Mayor et
al., 2007). Seven loci sequenced (efp, metG, pgiB, recA, adk, rpoB and tpiA)
Myxococcus xanthus
A previous study provided evidence that populations of this soil bacterium are unstructured
below a scale of 102 – 103 km (Vos and Velicer, 2008) and so all distinct ST’s collected
below such a regional scale (SW Germany) were used. Five loci were sequenced (clpX, csgA,
fibA, icd and sglK).
Neisseria lactamica
Seven loci (abcZ, adk, aroE, fumC, gdh, pdhC and pgm) were analyzed in isolates from
around the world (www.pubmlst.net).
Neisseria meningitides
Commensal, non-disease associated STs from the Czech republic (Jolley et al., 2005). Loci as
in N. lactamica.
Oenococcus oeni
6
Isolates from a variety of wine industry strain collections from all over the world (de Las
Rivas et al., 2004). Five loci analyzed (gyrB, ddl, pgm, recP and mleA).
Pelagibacter ubique (SAR 11)
Isolated from a 2 liter sample of sea water collected of the Oregon Coast. Eight loci used
(HSP60, ATPDH, ACoAAT, recA, OR, DPoIIIα, RPoIβ). A variety of tests, including the
coalescent-based program LDHat, provide strong evidence of very high recombination rates
in the original paper (Vergin et al., 2007).
Plesiomonas shigelloides
Five loci sequenced (fusA, leuS, pyrG, recG and rpoB). Isolates from, sewage, lakes, rivers
and a variety of animals. Only European isolates used for the analysis. Evidence for extensive
recombination presented in the original publication (Salerno et al., 2007).
Porphyromonas gingivalis
Global collection of periodontal pathogens. Seven loci sequenced (gdpxJ, pga, hagB, mcmA,
recA, ftsQ and pepO). No tests for recombination in the original publication (Enersen et al.,
2006).
Pseudomonas syringae
A collection of isolates from the foliage of a range of plant species. Isolates from across the
world, but little evidence of spatial structuring (Sarkar and Guttman, 2004). Four loci
sequenced (gapA, gltB, gyrB and rpoD). Sequences of additional strains provided by D.
Guttman.
Pseudomonas viridiflava
Most isolates from the USA, some European isolates included as well (the original
publication reports little geographic clustering) (Goss et al., 2005). Isolates found on a variety
7
of host plants. Three loci sequenced (gyrB, purA and aputative radical sterile alpha motif
domain protein).
Ralstonia solanacearum
Worldwide collection isolated from a variety of crops (Castillo and Greenberg, 2007). Seven
loci sequenced (gyrB, adk, gdhA, gapA, ppsA and fliC).
Rhizobium gallicum
R. gallicum sensu lato Group I strains isolated from around the northern hemisphere (Silva et
al., 2005). Three loci sequenced (glnII, atpD and nodB).
Salmonella enterica
The first 50 european isolates from the http://web.mpiib-berlin.mpg.de/mlst database. Seven
loci sequenced (aroC, dnaN, hemD, hisD, purE, sucA and thrA). High recombination rate is in
accordance with data on Salmonella enterica subspecies I (Octavia and Lan, 2006).
Staphylococcus aureus
Clinical isolates from Oxfordshire (Enright et al., 2000). Seven loci sequenced (arcC, aroE,
glpF, gmk, pta, tpi and yqiL).
Streptococcus pneumoniae
A distinct clade (Group 1 in (Hanage et al., 2005)) of typeable and nontypeable strains from
middle ear fluid and the nasopharynx. Six loci used (aroE, gdh, gki, recP, spi and xpt).
Streptococcus pyogenes
Group A Streptococci (GAS) are predominantly human pathogens. Seven loci (gki, gtr, murl,
mutS, recP, xtp and yqiL) were sequenced in upper respiratory tract-, invasive- and impetigo
isolates from the USA (the first 50 ST’s listed in the original study (Enright et al., 2001)).
8
Sulfolobus islandicus
Isolates from two hot springs (approx. 25 m apart) near the Mutnovsky Volcano on the
Kamchatka peninsula (Whitaker et al., 2005). Five loci used (hypothetical molydobterine
oxidoreductase, hypothetical acetyl Coa acetyl-transferase, hypothetical thermosome gamma
subunit, hypothetical transcription initiation factor and putative ATP-dependent helicase) (one
locus excluded because of evidence for selection).
Vibrio parahaemolyticus
A subset of 20 environmental isolates from the United States Pacific Coast was analyzed.
Seven loci (dnaE, gyrB, recA, dtdS, pntA, pyrC and tnaA) present on both chromosomes were
used. The original paper (Gonzalez-Escalona et al., 2008) reports high recombination rates on
the basis of a variety of tests.
Vibrio vulnificus
A distinct clade of mainly environmental isolates from around the world (Bisharat et al.,
2007). Five loci from the larger chromosome used (glp, gyrB, mdh, metG and purM).
Wolbachia b complex
Five loci sequenced (gatB, coxA, hcpA, fbpA and ftsZ) in symbionts from a variety of hosts
(Baldo et al., 2006). Insects can host multiple Wolbachia strains and strains are not limited to
a single host species. Classification of strains into species is still unresolved. The analysis was
performed on MLST complex b (with strains sharing minimal 3 identical alleles). Several
studies have documented homologous recombination in this species (Baldo et al., 2006;
Baldo et al., 2006; Jiggins et al., 2001).
Yersinia pseudotuberculosis
9
Isolates from Asia isolated from humans, animals and vegetables. Seven loci sequenced (adk,
argA, aroA, glnA, thrA, tmk and trpE); sequences from http://web.mpiib-berlin.mpg.de/mlst/.
B. Excluded Datasets
Several datasets were excluded because credibility intervals were extremely wide and so
mean r/m was not informative:
Acinetobacter baumannii: Clinical isolates from four European countries as well as several
reference strains (Bartual et al., 2005). Seven loci sequenced (gltA, gyrB, gdhB, recA, cpn60,
gpi and rpoD).
Burkholderia amfibaria: Eleven isolates from maize rhizosphere, Italy (Dalmastri et al.,
2007). Seven loci sequenced (atpB, gltB, gyrB, recA, lepA, phaC and trpB).
Burkholderia multivorans: Worldwide collection of mainly pathogenic (CF lung) strains
(www.pubmlst.net). Loci as in B. amfibaria.
Lactobacillus plantarum: Isolates collected in different countries, in different years (as far
back as 1948) from different sources (wine, foods, saliva, silage) (de Las Rivas et al., 2006).
(Sample thus not representative of a natural population.) Six loci sequenced (pgm, ddl, gyrB,
purK1, gdh and mutS).
Pseudomonas aeruginosa: The set consists of the first 50 ST’s from the UK archived at
www.pubmlst.net. Mainly from clinical samples, with several environmental isolates. Seven
loci sequenced (acsA, aroE, guaA, mutL, nuoD, ppsA and trpE) (Curran et al., 2004).
10
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17