Xylella fastidiosa: bacterial parasitism with hallmarks of commensalism

Roper, M. Caroline; Castro, Claudia; Ingel, Brian

doi:10.1016/j.pbi.2019.05.005

Cited by 43 publications

(42 citation statements)

References 49 publications

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“…In such a scenario, the fastidious behavior could be viewed as a developmental strategy of the pathogen to remain at a low population level inside the host and avoid detection by its immune system. This hypothesis is in agreement with the view of Xylella as a "self-limiting" organism, which has many features of a plant commensal but accidentally provokes epidemics due to an exaggerated and late plant response (64), probably linked to specific environmental conditions.…”

Section: Discussionsupporting

confidence: 90%

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

et al. 2020

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High proliferation rate and robustness are vital characteristics of bacterial pathogens that successfully colonize their hosts. The observation of drastically slow growth in some pathogens is thus paradoxical and remains unexplained. In this study, we sought to understand the slow (fastidious) growth of the plant pathogen Xylella fastidiosa. Using genome-scale metabolic network reconstruction, modeling, and experimental validation, we explored its metabolic capabilities. Despite genome reduction and slow growth, the pathogen’s metabolic network is complete but strikingly minimalist and lacking in robustness. Most alternative reactions were missing, especially those favoring fast growth, and were replaced by less efficient paths. We also found that the production of some virulence factors imposes a heavy burden on growth. Interestingly, some specific determinants of fastidious growth were also found in other slow-growing pathogens, enriching the view that these metabolic peculiarities are a pathogenicity strategy to remain at a low population level. IMPORTANCE Xylella fastidiosa is one of the most important threats to plant health worldwide, causing disease in the Americas on a range of agricultural crops and trees, and recently associated with a critical epidemic affecting olive trees in Europe. A main challenge for the detection of the pathogen and the development of physiological studies is its fastidious growth, as the generation time can vary from 10 to 100 h for some strains. This physiological peculiarity is shared with several human pathogens and is poorly understood. We performed an analysis of the metabolic capabilities of X. fastidiosa through a genome-scale metabolic model of the bacterium. This model was reconstructed and manually curated using experiments and bibliographical evidence. Our study revealed that fastidious growth most probably results from different metabolic specificities such as the absence of highly efficient enzymes or a global inefficiency in virulence factor production. These results support the idea that the fragility of the metabolic network may have been shaped during evolution to lead to the self-limiting behavior of X. fastidiosa.

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Section: Discussionsupporting

confidence: 90%

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

et al. 2020

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“…In the host plant, Xf colonizes the xylem vessels and elicits their occlusion [11,23,32]. Xf maintains a lifestyle that switches bidirectionally from adhesive to non-adhesive cells phenotype and vice versa [14]. Lipids are crucial signals that can modulate the pathogen virulence and play important roles during the infection process [15,33].…”

Section: Discussionmentioning

confidence: 99%

“…Our working hypothesis on the effects of these compounds on Xf biofilming stemmed from the available information on their biological role and was inspired by Roper and colleagues' intuition: "the bacteria induce an autoimmune-like syndrome" [14]. More specifically, the oleic acid is among the modulators of quorum sensing in Xf [15]; in other bacterial pathogens…”

Section: Plos Onementioning

confidence: 99%

“…From the point of entry in grapevine, Xf moves along the xylem, attaches to its walls and, through a tight coordination of the adherent biofilm and the planktonic states, invades the host systemically [12,13]. The planktonic phase is correlated to low cell density and vessel colonization [14]. The colonization during the exploratory phase (planktonic) is correlated to low cell density and symptoms progression in grapevine.…”

Section: Introductionmentioning

confidence: 99%

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Xylella fastidiosa subsp. pauca and olive produced lipids moderate the switch adhesive versus non-adhesive state and viceversa

Scala¹,

Pucci²,

Salustri

et al. 2020

PLoS ONE

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Global trade and climate change are reshaping the distribution map of pandemic pathogens. One major emerging concern is Xylella fastidiosa, a tropical bacterium recently introduced into Europe from America. In last decades, X. fastidiosa was detected in several European countries. X. fastidiosa is an insect vector-transmitted bacterial plant pathogen associated with severe diseases in a wide range of hosts. X. fastidiosa through a tight coordination of the adherent biofilm and the planktonic states, invades the host systemically. The planktonic phase is correlated to low cell density and vessel colonization. Increase in cell density triggers a quorum sensing system based on mixture of cis 2-enoic fatty acidsdiffusible signalling factors (DSF) that promote stickiness and biofilm. The lipidome profile of Olea europaea L. (cv. Ogliarola salentina) samples, collected in groves located in infected zones and uninfected zones was performed. The untargeted analysis of the lipid profiles of Olive Quick Decline Syndrome (OQDS) positive (+) and negative (-) plants showed a clustering of OQDS+ plants apart from OQDS-. The targeted lipids profile of plants OQDS+ and OQDS-identified a shortlist of 10 lipids that increase their amount in OQDS+ and X. fastidiosa positive olive trees. These lipid entities, provided to X. fastidiosa subsp. pauca pure culture, impact on the dual phase, e.g. planktonic $ biofilm. This study provides novel insights on OQDS lipid hallmarks and on molecules that might modulate biofilm phase in X. fastidiosa subsp. pauca.

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“…From the point of entry in grapevine, Xf moves along the xylem, attaches to its walls and, through a tight coordination of the adherent biofilm and the planktonic states, invades the host systemically [12,13]. The planktonic phase is correlated to low cell density and vessel colonization [14]. Increase in cell density triggers a quorum sensing system based on cis 2-enoic fatty acids—diffusible signalling factors (DSF) that promote stickiness and biofilm [15].…”

Section: Introductionmentioning

confidence: 99%

Bacterial and plant produced lipids can exacerbate the Olive Quick Decline Syndrome caused byXylella

Pucci¹,

Salustri

Modesti³

et al. 2019

Preprint

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25Xylella fastidiosa is an insect vector-transmitted bacterial plant pathogen associated with severe 26 diseases in a wide range of plants. In last decades, X. fastidiosa was detected in several European 27 countries. Among X. fastidiosa subspecies, here we study X. fastidiosa subsp. pauca associated with 28 the Olive Quick Decline Syndrome (OQDS) causing severe losses in Southern Italy. First, we 29 collected Olea europaea L. (cv. Ogliarola salentina) samples in groves located in infected zones and 30 uninfected zones. Secondly, the untargeted LC-TOF analysis of the lipid profiles of OQDS positive 31 (+) and negative (-) plants showed a significant clustering of OQDS+ samples apart from OQDS-32 ones. Thirdly, using HPLC-MS/MS targeted methods and chemometric analysis, we identified a 33 shortlist of 10 lipids significantly different in the infected versus healthy samples. Last, we observed 34 a clear impact on X. fastidiosa subsp. pauca growth and biofilm formation in vitro liquid cultures 35supplemented with these compounds. 36Considering that growth and biofilm formation are primary ways by which X. fastidiosa causes 37 disease, our results demonstrate that lipids produced as part of the plant's immune response can 38 exacerbate the disease. This is reminiscent of an allergic reaction in animal systems, offering the 39 depression of plant immune response as a potential strategy for OQDS treatment. 40Author summary 41 Global trade and climate change are re-shaping the distribution map of pandemic pathogens. One 42 major emerging concern is Xylella fastidiosa, a tropical bacterium recently introduced into Europe 43 from America. Its impact has been dramatic: in the last 5-years only, Olive Quick Decline Syndrome 44 (OQDS) has caused thousands of 200 years old olive trees to be felled in the southern Italy. Xylella 45 fastidiosa through a tight coordination of the adherent biofilm and the planktonic states, invades the 46 host systemically. The planktonic phase is correlated to low cell density and vessel colonization. 47 Increase in cell density triggers a quorum sensing system based on cis 2-enoic fatty acids-diffusible 48 signalling factors (DSF) that promote stickiness and biofilm. Xylem vessels are occluded by the 49 3combined effect of bacterial biofilm and plant defences (e.g. tyloses). This study provides novel 50 insight on how X. fastidiosa subsp. pauca biology relates to the Olive Quick Decline Syndrome. We 51 found that some class of lipids increase their amount in the infected olive tree. These lipid entities, 52 provided to X. fastidiosa subsp. pauca behave as hormone-like molecules: modulating the dual phase, 53 e.g. planktonic versus biofilm. Probably, part of these lipids represents a reaction of the plant to the 54 bacterial contamination. 55

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Xylella fastidiosa: bacterial parasitism with hallmarks of commensalism

Cited by 43 publications

References 49 publications

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

Xylella fastidiosa subsp. pauca and olive produced lipids moderate the switch adhesive versus non-adhesive state and viceversa

Bacterial and plant produced lipids can exacerbate the Olive Quick Decline Syndrome caused byXylella

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