What makes Xanthomonas albilineans unique amongst xanthomonads? [original]

MINI REVIEW

published: 24 April 2015

doi: 10.3389/fpls.2015.00289

Edited by:

Nicolas Denancé,

Institut National de la Recherche

Agronomique, France

Reviewed by:

Joao C. Setubal,

University of Sao Paulo, Brazil

Julian J. Smith,

Fera Science Ltd., UK

*Correspondence:

Stéphane Cociancich,

UMR BGPI, Cirad, TA A-54/K,

Campus international de Baillarguet,

F-34398 Montpellier Cedex 5, France

[email protected]

Specialty section:

This article was submitted to

Plant-Microbe Interaction,

a section of the journal

Frontiers in Plant Science

Received: 24 February 2015

Accepted: 09 April 2015

Published: 24 April 2015

Citation:

Pieretti I, Pesic A, Petras D, Royer M,

Süssmuth RD and Cociancich S

(2015) What makes Xanthomonas

albilineans unique amongst

xanthomonads?

Front. Plant Sci. 6:289.

doi: 10.3389/fpls.2015.00289

What makes Xanthomonas

albilineans unique amongst

xanthomonads?

Isabelle Pieretti 1, Alexander Pesic 2, Daniel Petras 2, Monique Royer 1,

Roderich D. Süssmuth 2and Stéphane Cociancich 1*

1UMR BGPI, Cirad, Montpellier, France, 2Institut für Chemie, Technische Universität Berlin, Berlin, Germany

Xanthomonas albilineans causes leaf scald, a lethal disease of sugarcane. Compared to

other species of Xanthomonas, X. albilineans exhibits distinctive pathogenic mechanisms,

ecology and taxonomy. Its genome, which has experienced significant erosion, has

unique genomic features. It lacks two loci required for pathogenicity in other plant

pathogenic species of Xanthomonas: the xanthan gum biosynthesis and the Hrp-T3SS

(hypersensitive response and pathogenicity-type three secretion system) gene clusters.

Instead, X. albilineans harbors in its genome an SPI-1 (Salmonella pathogenicity island-1)

T3SS gene cluster usually found in animal pathogens. X. albilineans produces a potent

DNA gyrase inhibitor called albicidin, which blocks chloroplast differentiation, resulting in

the characteristic white foliar stripe symptoms. The antibacterial activity of albicidin also

confers on X. albilineans a competitive advantage against rival bacteria during sugarcane

colonization. Recent chemical studies have uncovered the unique structure of albicidin

and allowed us to partially elucidate its fascinating biosynthesis apparatus, which involves

an enigmatic hybrid PKS/NRPS (polyketide synthase/non-ribosomal peptide synthetase)

machinery.

Keywords: Xanthomonas albilineans, leaf scald disease of sugarcane, genomic features, albicidin, NRPS and PKS

genes

Introduction

Xanthomonas albilineans (Ashby) Dowson is known to invade the xylem of sugarcane and to

cause leaf scald disease (Rott and Davis, 2000; Birch, 2001). Symptoms of this disease vary from

a single, white, narrow, sharply defined stripe to complete wilting and necrosis of infected leaves,

leading to plant death. Dissemination of X. albilineans occurs mainly mechanically through use of

contaminated harvesting tools and by distribution and planting of infected cuttings. However, aerial

transmission and potential for epiphytic survival have also been reported for this pathogen (Autrey

et al., 1995; Daugrois et al., 2003; Champoiseau et al., 2009).

Xanthomonas albilineans is a representative of the genus Xanthomonas, members of which

are exclusively Gram-negative plant-associated bacteria that collectively cause dramatic damage to

hundreds of plant species of ornamental or agronomical interest. Indeed, both monocotyledonous

(e.g., rice, sugarcane, or banana) and dicotyledonous (e.g., citrus, cauliflower, bean, pepper, cabbage,

and tomato) plants are targeted worldwide by various Xanthomonas species. While sharing numerous

phenotypic characteristics, at least 27 species and over 120 pathovars (variants of pathogeny)

of the genus Xanthomonas are currently recognized. Each pathovar individually exhibits a very

Frontiers in Plant Science | www.frontiersin.org April 2015 | Volume 6 | Article 2891

Pieretti et al. Specific features of Xanthomonas albilineans

restricted host range and/or tissue-specificity and this leads to

clustering of bacterial strains causing similar symptoms on the

same host.

Multilocus sequence analysis (MLSA) with four housekeeping

genes resulted in the distribution of Xanthomonas species in two

clades. The main one contains the majority of species whereas the

secondary clade contains X. albilineans,Xanthomonas sacchari,

Xanthomonas theicola,Xanthomonas hyacinthi, and Xanthomonas

translucens (Young et al., 2008). Phylogenetic analyses with the

gyrB sequence indicate that this secondary group also contains

several uncharacterized species of Xanthomonas isolated mainly

on rice, banana or sugarcane (Studholme et al., 2011, 2012).

Intriguingly, two multiMLSA studies with 28 genes and 228 genes,

respectively, in which X. albilineans is the only representative of

this secondary clade, resulted in the branching of Xylella fastidiosa

between X. albilineans and the main clade (Rodriguez-R et al.,

2012; Naushad and Gupta, 2013). X. fastidiosa is a xylem-limited

bacterium which is insect-vectored to a variety of diverse hosts,

has a reduced genome and lacks the Hrp-T3SS (hypersensitive

response and pathogenicity–type III secretion system; Simpson

et al., 2000).

Analysis of the X. albilineans genome has revealed unusual

features compared to other xanthomonads, the most prominent

being the absence of the Hrp-T3SS gene cluster and the occurrence

of genome erosion. Furthermore, to our knowledge, X. albilineans

is the only xanthomonad that produces the phytotoxin albicidin.

This mini-review aims to summarize the characteristics that,

taken together, make X. albilineans so unique.

Genome Erosion

The genome of X. albilineans strain GPE PC73 has been fully

sequenced and annotated. It consists of a 3,768,695-bp circular

chromosome with a G+C content of 63%, and three plasmids of

31,555-bp, 27,212-bp and 24,837-bp, respectively (Pieretti et al.,

2009). This genome size is much smaller than that of any other

xanthomonad sequenced to date (commonly ∼5 Mb). Examina-

tion of the genome of strain GPE PC73 together with OrthoMCL

comparative analyses performed with other sequenced xan-

thomonads highlights several genomic features that distinguish

X. albilineans from its near relatives (Pieretti et al., 2009, 2012;

Marguerettaz et al., 2011; Royer et al., 2013).

Orthologous analyses show that X. albilineans and X. fastidiosa

have experienced a convergent genome reduction during their

respective speciation, with a more extensive genome reduction

for X. fastidiosa (Pieretti et al., 2009). Based on these analyses,

X. albilineans has lost at least 592 genes that were present in the

last common ancestor of the xanthomonads. Interestingly, most of

these ancestral genes are conserved in the genome of X. sacchari

strains NCPPB4393 and LMG 476 and Xanthomonas spp. strains

NCPPB1131 and NCPPB1132, which are the sequenced strains

phylogenetically closest to X. albilineans (Studholme et al., 2011,

2012; Pieretti et al., 2015). This indicates that genome erosion

is specific to X. albilineans. Convergent genome erosion of X.

albilineans and X. fastidiosa could be linked to a similar adaptation

to a xylem-invading lifestyle in which interactions with living

plant tissues are minimal (Pieretti et al., 2009). More recently, a

study of the somewhat reduced genome of Xanthomonas fragariae

(4.2 Mb) led to the hypothesis that the convergent genome reduc-

tion observed in some xanthomonads could be linked to their

endophytic lifestyle and typically to their commitment to a single

host (Vandroemme et al., 2013).

Compared to other xanthomonads, a low number of insertion

sequences (IS) has been found in the genome of X. albilineans.

Taken together with a limited recombination of the chromosome

and a GC skew pattern containing a low number of distortions, it

was postulated that genome erosion of X. albilineans was mainly

not due to IS and other mechanisms were proposed for this

erosion (Pieretti et al., 2009). The low number of IS could be linked

to the activity of CRISPR (clustered regularly interspaced short

palindromic repeats) systems. Strain GPE PC73 of X. albilineans

possesses two CRISPR loci. The first one, CRISPR-1, is conserved

in X. oryzae pv. oryzae,X. axonopodis pv. citri,X. campestris

pv. vasculorum, and X. campestris pv. musacearum. The second,

CRISPR-2, is present in X. campestris pv. raphani (Pieretti et al.,

2012). Interestingly, many spacers of CRISPR-1 and CRISPR-2

of strain GPE PC73 are identical to IS or phage-related DNA

sequences present on the chromosome of this strain (Pieretti et al.,

2012).

Specific Genes Linked to a Xylem-Invading

Lifestyle

Although determinants for host- or tissue-specificity of X. albilin-

eans remain unclear, the presence in its genome of genes encoding

cell-wall-degrading enzymes (CWDEs) with specific features is

probably important for its ability to spread in xylem and for

pathogenicity. Indeed, all CWDEs from X. albilineans harbor a

cellulose-binding domain (CBD) and a long linker region both

adapted to the utilization of cell-wall breakdown products as

carbon source and to the ability to spread in sugarcane xylem

vessels (Pieretti et al., 2012). These enzymes may also be required

to disrupt pit membranes in sugarcane, thereby promoting prop-

agation of the bacteria in the plant. Interestingly, X. fastidiosa also

encodes two CWDEs containing a long linker and a CBD. It has

been shown that one of these two CWDEs is involved in the spread

of X. fastidiosa in the xylem by increasing the pore size of pit

membranes. CWDEs are therefore considered as virulence factors

(Roper et al., 2007; Chatterjee et al., 2008; Pérez-Donoso et al.,

2010). TonB-dependent transporters (TBDTs) may be used by

X. albilineans to transport cell-wall-degrading products resulting

from the activity of CWDEs, and thus may facilitate spread of the

organism in the nutrient-poor conditions prevailing in the xylem

of sugarcane. In the genome of X. albilineans, 35 TBDT genes

have been identified, including one specific to this species and

two others that are functionally associated to pathogenicity of the

bacterium (Rott et al., 2011; Pieretti et al., 2012).

Lack of Hrp-T3SS

Most phytopathogenic bacteria rely on the type III secretion

system (T3SS) of the hypersensitive response and pathogenicity

family (Hrp1 and Hrp2, respectively). This syringe-like apparatus

allows pathogens to deliver, into their host cells, proteins (type

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Pieretti et al. Specific features of Xanthomonas albilineans

III effectors) that modulate plant physiology and immunity for

the benefit of the pathogen. Interestingly, genes encoding the

injectisome and associated effectors of the Hrp-T3SS are missing

in the genome of X. albilineans, as is also the case in the genomes of

X. sacchari strains NCPPB4393 and LMG 476 and Xanthomonas

spp. strains NCPPB1131 and NCPPB1132 (Studholme et al., 2011,

2012; Pieretti et al., 2015). Yet, an Hrp system is present in

other close neighbor species of X. albilineans, such as X. translu-

cens pv. graminis strain 29, X. translucens pv. translucens strain

DSM18974, and X. translucens strain DAR 61454 (Wichmann

et al., 2013; Gardiner et al., 2014). Although the Hrp-T3SS is

described as a crucial key component in plant–host interactions

for most Xanthomonas spp, it seems not to be essential in X.

translucens pv. graminis strain 29 for xylem colonization, even

though it is involved in symptom development (Ryan et al., 2011;

Wichmann et al., 2013). Similarly, despite being devoid of any Hrp

T3SS, X. albilineans displays pathogenicity and is able to cause

serious damage to sugarcane.

Acquisition of a SPI-1 T3SS

The annotated sequence of the genome of X. albilineans strain

GPE PC73 reveals the presence of a T3SS belonging to the

Salmonella pathogenicity island-1 (SPI-1) injectisome family.

Genes encoding this system are located near the terminus of the

replication site of the chromosome and were probably acquired

by lateral gene transfer. This secretion system, found mainly in

mammals and insects bacterial pathogens or symbionts, exhibits

high similarity to that described in Burkholderia pseudomallei—a

human pathogen causing melioidosis (Stevens et al., 2002). The

SPI-1 needle-like assemblies of X. albilineans strain GPE PC73 and

B. pseudomallei strain K96243 are homologous. Both species share

all but two genes—orgA and orgB, encoding putative oxygen-

regulated invasion proteins involved in type three secretion that

are not conserved in B. pseudomallei. The genome composi-

tion of the SPI-1 T3SS in X. albilineans additionally includes

genes encoding translocon components (xipB,xipC, and xipD),

injectisome components (xsaJ to xsaS and xsaV to xsaZ) and a

chaperone (xicA). Furthermore, the locus contains 15 additional

genes referred to as xapA–xapO, encoding hypothetical proteins.

These genes, which show homology neither to sequences from

B. pseudomallei nor to sequences available from protein sequence

databases, are specific to X. albilineans and their products repre-

sent good candidates to be considered as effectors for this SPI-1

T3SS (Marguerettaz et al., 2011). Interestingly, this SPI-1 T3SS is

conserved in Xanthomonas axonopodis pv. phaseoli strains CFBP

2534, CFBP 6164 and CFBP 6982, which moreover possess a

second T3SS belonging to the Hrp2 family (Alavi et al., 2008;

Marguerettaz et al., 2011). Pathogenicity of X. albilineans strains

seems not to be linked to the presence of the SPI-1 T3SS in

their genome; besides, no SPI-1 T3SS locus has been identified

in strain PNG130 of X. albilineans even though it is able to

spread in sugarcane. Functional analyses showed that, in planta,

multiplication of a SPI-1 T3SS knockout mutant of X. albilineans

was not impaired when compared to the wild-type, indicating

that the SPI-1 T3SS is not required for spread in sugarcane

vessels or for development of leaf scald symptoms. The role of

the SPI-1 T3SS of X. albilineans remains unclear, although it

has been conserved during its evolution in X. albilineans with-

out frame-shifting indels or nonsense mutations (Marguerettaz

et al., 2011). It remains possible, in conditions other than those

tested with our knockout mutant, that the SPI-1 T3SS system

may be required for interaction with sugarcane, as in the case of

SPI-1 of Salmonella, which is involved in interactions with Ara-

bidopsis thaliana (Schikora et al., 2011). The SPI-1 T3SS system

may also be associated with other aspects of the X. albilineans

lifestyle, e.g., an involvement in adherence as reported for Erwinia

tasmaniensis (Kube et al., 2008) or in formation of pellicle or

biofilm-like structures (Jennings et al., 2012), which could be

related to epiphytic survival on sugarcane leaves. Although no

insect vector has been identified for X. albilineans to date, we

cannot rule out that the SPI-1 T3SS could be involved in insect

association or might mediate persistence of the bacterium in an

insect vector as was shown for Pantoea stewartii (Correa et al.,

2012).

Lack of T6SS and the Xanthan Gum Gene

Cluster

Xanthomonas albilineans lacks two other major pathogenicity

factors that are common features of most xanthomonads. First,

it lacks the gum gene cluster for extracellular polysaccharide

(EPS) synthesis. This gene cluster is responsible for biofilm and

xanthan gum formation, and is associated with pathogenesis in

xanthomonads (Katzen et al., 1998; Kim et al., 2009; Galván et al.,

2012). Exceptions are X. fragariae, which lacks the gumN,gumO

and gumP genes, and X. albilineans, which lacks the complete set

of gum genes, indicating those are not essential for virulence of

both these pathogens (Pieretti et al., 2012; Vandroemme et al.,

2013).

Xanthomonas albilineans is also devoid of any type VI secre-

tion system (T6SS) described in other xanthomonads, as for

example in Xanthomonas fuscans pv. fuscans strain 4834-R and

Xanthomonas citri subsp. citri strain 306, which each contain a

single T6SS (Potnis et al., 2011; Darrasse et al., 2013) or X. translu-

cens strain DAR61454, which encodes two distinct T6SS (Gar-

diner et al., 2014). Structurally, the T6SS looks like an inverted

bacteriophage. Functionally, this system is able to interact with

both eukaryotic and prokaryotic cells by delivering effectors or

toxins into host cells to subvert the signaling process to its own

advantage, but also into other bacteria from the same habitat to

outcompete them during infection (Filloux, 2013; Russell et al.,

2014). Despite its multifunctional roles during host–pathogen

interactions, the lack of T6SS in Xanthomonas campestris pv.

campestris strain 8004, Xanthomonas gardneri strain 101, and

X. albilineans seems to have no effect on pathogenesis of these

xanthomonads.

Albicidin and Other Non-Ribosomally

Synthesized Peptides

A unique feature of X. albilineans is the production of albi-

cidin—a phytotoxin causing the white foliar stripe symptoms

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Pieretti et al. Specific features of Xanthomonas albilineans

FIGURE 1 | Xanthomonas albilineans produces the phytotoxin

albicidin—a potent gyrase inhibitor that blocks chloroplast

differentiation, resulting in sugarcane leaf scald disease

symptoms. (A) Structure of albicidin, a hybrid PKS/NRPS compound

with unique composition including p-aminobenzoic acid and

cyanoalanine. (B) Diseased sugarcane plant with characteristic leaf scald

symptoms: white foliar bleaching and necrosis of infected leaves

characteristic of leaf scald disease of sugarcane (Birch and Patil,

1985). Albicidin is a potent DNA gyrase inhibitor that blocks the

differentiation of chloroplasts (Figure 1). It also targets bacterial

gyrase by a mechanism different from that of other DNA gyrase

inhibitors like coumarins and quinolones (Hashimi et al., 2007).

This mode of action accounts for the potent antibacterial activity

of albicidin, which inhibits the growth of Gram-positive and

Gram-negative pathogenic bacteria at nanomolar concentrations

(Birch and Patil, 1985). Albicidin gives a competitive advantage

to X. albilineans against other bacteria within the xylem vessels

of sugarcane (Magnani et al., 2013). Interestingly, two sugarcane-

living bacteria harbor an albicidin resistance gene: Leifsonia xyli

(Monteiro-Vitorello et al., 2004) and Pantoea dispersa (Zhang and

Birch, 1997).

Albicidin is produced by a hybrid polyketide synthase

(PKS)/non-ribosomal peptide synthetase (NRPS) enzyme com-

plex. PKS and NRPS genes are often clustered together with a large

set of regulatory, transport or modification (tailoring) genes, as

well as genes involved in the biosynthesis of non-proteinogenic

amino acids. In addition to a phosphopantetheinyl transferase

required for activation of the PKS/NRPS system and a HtpG

chaperone, the role of which remains unclear, a locus (alb cluster)

containing 20 genes is required for albicidin biosynthesis. Among

these 20 genes, 3 encode the PKS/NRPS system; 15 others act

as transport, regulatory, modification or resistance genes (Royer

et al., 2004).

Non-ribosomal peptide synthetases are multimodular mega-

synthetases used by bacteria and fungi to produce peptides in a

ribosome-independent manner (Strieker et al., 2010). Each mod-

ule governs the specific incorporation of an amino acid substrate

based on signature sequences in the adenylation (A) domains

(Stachelhaus and Marahiel, 1995), which are loaded onto pep-

tidyl carrier protein (PCP) domains. Elongation of the peptide

is mediated by condensation (C) domains present within each

module. PKSs function according to the principles of fatty acid

biosynthesis (Weissman and Leadlay, 2005).

For decades, the structure elucidation of albicidin was impeded

by its extremely low production yield by X. albilineans. A first

step to overcome this bottleneck was achieved by transferring the

biosynthetic genes into a heterologous host, namely X. axonopodis

pv. vesicatoria, resulting in a significant increase in albicidin

production (Vivien et al., 2007). Extensive HPLC purification of

albicidin and thorough analysis of the purified compound by

means of mass spectrometry and nuclear magnetic resonance

spectroscopy then allowed us to unravel its unique structure

(Figure 1). Albicidin proved to be a linear pentapeptide composed

of cyanoalanine and p-amino benzoic acids N-terminally linked to

ap-coumaric acid derivative (Cociancich et al., 2015). Although

over 500 different monomers (amino acid substrates) have been

identified to date as being incorporated by NRPS systems, eluci-

dation of the structure of albicidin revealed for the first time the

incorporation by NRPSs of cyanoalanine and p-amino benzoic

acids. Moreover, the incorporation of p-amino benzoic acids is the

first example of incorporation of a δ-aminoacid by NRPSs, since

all NRPSs described to date incorporate only αor βaminoacids.

The use of unusual amino acid substrates is linked to unique

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Pieretti et al. Specific features of Xanthomonas albilineans

features that were identified in silico 10 years ago within the

albicidin NRPS modules sequence (Royer et al., 2004). The forma-

tion and incorporation of cyanoalanine most likely occurs in situ

through an additional module present in the PKS-NRPS assembly

line that was investigated in one of our present studies (Cociancich

et al., 2015).

Chemical synthesis of albicidin is now available, allowing both

production of high quantities of the compound for further study

of its mode of action and activity spectrum, and the synthesis of

analogs (Kretz et al., 2015). The uniqueness of its structure and the

specific mode of action of this compound make albicidin a strong

lead structure for antibiotic development.

Data mining of the genome of X. albilineans strain GPE PC73

has led to the identification, in addition to the albicidin biosyn-

thesis locus, of five other NRPS loci (Pieretti et al., 2012; Royer

et al., 2013). The first, named Meta-B, encodes megasynthases

performing peptidic elongation of a 16-amino acid lipopeptide.

This locus also encodes a transcription regulator belonging to the

AraC family, a cyclic peptide transporter, and enzymes involved

in biosynthesis of the non-proteinogenic amino acids di-amino

butyric acid and dihydroxyphenylglycine. Interestingly, the NRPS

locus Meta-B has been identified in the genome of strains of

three other Xanthomonas species, namely Xanthomonas oryzae pv.

oryzae strains BAI3 and X11-5A, X. translucens strain DAR61454

and Xanthomonas spp. strain XaS3 (Royer et al., 2013). Despite

a similar organization of the genes within these loci, the in silico

prediction of the sequences of the peptides produced indicates that

each strain produces a different lipopeptide.

Two other NRPS gene clusters, Meta-A and Meta-C, have been

identified in the genome of X. albilineans strain GPE PC73. They

encode megasynthases that perform the biosynthesis of peptides

of 12 and 7 amino acids, respectively. A partial sequence has been

predicted for each of these peptides (Royer et al., 2013).

Finally, two short NRPS genes have also been identified on

the chromosome of X. albilineans: they both encode only one

NRPS module. Interestingly, there is an overlap between both

these genes and a gene encoding a glycosyltransferase. It has been

hypothesized that these genes encode glycosylated amino acids, to

which, however, no precise function could yet be attributed (Royer

et al., 2013).

Conclusion

Although most xanthomonads require pathogenicity factors such

as gum genes, T3SS Hrp and T6SS for survival, growth and spread

within host plants, X. albilineans lacks these pathogenicity factors,

de facto reducing its artillery to circumvent sugarcane defense

mechanisms and innate immunity. While being “disarmed” could

be disadvantageous for a vascular plant pathogen, X. albilineans

remains able to invade and spread in sugarcane, suggesting that

it uses other strategies, such as stealth, i.e., being unobtrusive

in planta, to minimize inducible host defense responses. On the

other hand, the reduced genome of X. albilineans has specific

features that may be involved in the adaptation of the bacterium

to live and spread in sugarcane xylem vessels. For example, spe-

cific CWDEs and TBDTs appear to be optimized for life in the

nutrient-poor sugarcane xylem environment. The uniqueness of

X. albilineans resides also in the production of the phytotoxin

and antibiotic albicidin. The recently unraveled structure and

concomitant development of a chemical synthesis protocol for

this compound leads to additional prospects for its use in the

antibiotherapy field. According to the specificities deriving from

the biological, biochemical, phylogenetic and genomic analyses

described in this review, one can truly say that X. albilineans is

quite unique amongst the genus Xanthomonas.

Acknowledgments

Work on albicidin was supported by a grant from the Deutsche

Forschungsgemeinschaft (DFG SU239/11-1; SU 18-1), by the

Cluster of Excellence “Unifying Concepts in Catalysis (UniCat)”

(DFG) and by a grant from the Agence Nationale de la Recherche

(ANR-09-BLAN-0413-01). The authors are indebted to Helen

Rothnie for English editing.

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