The Art of M. Nicole van Dam, in Grayscale

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The axonemal defect resulting in paralysis is a well-characterised disruption of the central pair in kinetoplastids Fig 3B and [ 23 , 54 , 55 ] and is similar to the defect of the pf16 Chlamydomonas reinhardtii mutant [ 56 ] indicating it is a well-conserved core axoneme component. Two days post blood-meal PBM , the L.


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In all lines, promastigotes were localized in the abdominal midgut, within the bloodmeal enclosed in the peritrophic matrix Fig 7B. At day 6 the infection rate was 7. This defect was rescued by restored expression of MBO2 Fig 7.

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Our data provide strong evidence that flagellum-driven directional motility is an essential requirement for successful Leishmania development in sand flies and, by implication, parasite transmission. Numbers above the bars indicate numbers of dissected females in the group. B Localization of L. Numbers above the bars indicate numbers of infected females in the group.

We first defined a flagellar proteome by pursuing a flagellar isolation protocol yielding a defined section of intact flagella and comparing both the flagella and the deflagellated cell body fractions to define a relative enrichment score for each protein. The SINQ method [ 25 , 27 , 28 ] eliminated from our analysis abundant cell body proteins that were likely cross-contaminants in the flagellar fractions.

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The flagellar proteins Fig 2 defined by this method showed similarities in numbers and types of proteins to other analyses of eukaryotic flagella and cilia S5 Fig , S4 Table , [ 5 ]. We also show the importance of directional flagellar motility in the colonisation of sand flies. The data from the pooled mutant population show a progressive loss of paralysed or uncoordinated swimmers over nine days from infection. MBO2 is an evolutionarily conserved axonemal protein [ 57 ] and derives its name from Chlamydomonas mutants that m ove b ackwards o nly because the algal flagella remain locked in a flagellar beat and cannot readily switch to a ciliary beat [ 58 ].

Taken together, these findings show that parasite motility is required for completion of the Leishmania life cycle, in line with the essential role of motility in other vector-transmitted protists. For example, Rotureau et al.

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It seems likely that loss of motility also contributed to the inability of L. The interesting question remains to what extent flagellar motility and attachment via the flagellum are linked. Observations of attached Leishmania in dissected sand flies show adhesion specifically via the flagellum but the precise molecular interactions between flagellum and the microvillar gut lining remain to be clarified.

The dominant cell surface glycoconjugate LPG which covers the entire parasite surface including the flagellum is known to be important in Leishmania attachment to sand fly guts [ 61 ] and our results support the view that LPG plays an important role in L. The consistency of the pooled mutant data with the reported phenotypes of individual glycoconjugate-deficient mutants demonstrates the power of this new rapid method for mutant phenotyping in Leishmania.

However, whilst a role for LPG in L. Zauli et al. These cells had a short flagellum barely protruding from the flagellar pocket, with an amorphous tip suggestive of a defect in flagellum elongation. In experimental infections of L. It would be interesting to follow up the subsequent development of this mutant in the fly. Interestingly, here only 1. It is possible that loss of directional motility impedes traversal of the peritrophic matrix and it would be informative to look for differences between mutants in the subsequent colonisation of the microvillar lining.

Several lines of evidence suggest a role for the trypanosomatid flagellum in environmental sensing [ 42 , 63 — 65 ]. Evidence for specific signal transduction pathways aiding promastigote navigation through the sand fly is however limited. Cyclic nucleotide signal transduction pathways may have important roles in coupling environmental sensing with regulation of flagellar beat patterns [ 66 , 67 ] and have been shown to be involved in the migration of T. Knockout of receptor-type adenylate cyclase a-like protein LmxM.

Perturbation of the flagellar membrane might be expected to interfere with sensory functions mediated through the flagellum. Ablation of membrane proteins LmxM. BBS2 is an integral part of the core BBSome complex which is highly conserved across ciliated eukaryotes [ 69 ] and functions as a cargo adaptor for ciliary membrane protein trafficking in Chlamydomonas flagella and metazoan cilia [ 70 ]. By contrast, KO of Kharon1, a protein shown to be required for trafficking of the glucose transporter LmGT1, and perhaps other proteins, to the promastigote flagellum [ 52 ] led to slightly reduced fitness in the flies from the earliest time point.

This is reminiscent of the previously published abortive phenotype of L. Failed attachment as a result of the shortened flagellum was thought to be a likely cause for the rapid clearance of Ld ARL-3A-Q70L-expressing parasites but it was noted that an inability to migrate at later stages of development would also lead to the disappearance of the mutants [ 60 ]. Arl-3A acts as guanine nucleotide exchange factor in the transport of lipidated proteins to the flagellar membrane [ 71 ] and protein mis-targeting could contribute to the phenotype in addition to flagellar shortening.

Further insights into the contribution of flagellar membrane proteins to attachment or directional swimming behaviour may be uncovered by further biochemical studies into flagellar membrane composition and subjecting different mutants with or without overt motility phenotypes in culture to chemotaxis assays and fly infections. Flagella isolated by the method used in this study provide suitable starting material for further targeted experiments to identify integral membrane proteins.

This could be achieved by using for example carbonate fractionation, as used for the enrichment of membrane proteins in olfactory cilia [ 72 ], or combining surface labelling with subsequent affinity purification prior to mass spectrometry [ 73 ].


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In contrast to the absolute requirement of motility for movement through the sand fly vector, flagellar motility is dispensable for promastigote proliferation in culture. Promastigotes are viable and able to divide even if they fail to assemble a flagellum at all, as demonstrated originally by the deletion of cytoplasmic dynein-2 heavy chain gene LmxDHC2. Thus, in Leishmania , flagellar mutant phenotypes can be observed in replication-competent cells over many cell cycles and our mutant library enables detailed systematic studies of KO phenotypes to probe protein functions in flagellum assembly, motility and signal transduction.

A fruitful area for further studies will be dissection of PFR function and assembly mechanisms.

The PFR comprises more than 40 proteins, some with structural roles, others with roles in adenine nucleotide homeostasis, cAMP signalling, calcium signalling and many uncharacterised components [ 76 , 77 ] and it may anchor metabolic and regulatory proteins as well as influencing the mechanical properties of the flagellum. Whether LmxM. Motility mutants analysed in our screen also included deletions of genes with human orthologs linked to ciliopathies such as hydin or male infertility CFAP43 and CFAP44 [ 78 ]. Leishmania offers a genetically tractable system to gain further mechanistic insight into their functions.

The hydin mutant has been extensively characterised in other species: in mammals, mutations in the hydin gene cause early-onset hydrocephalus [ 79 ] and subsequent studies on C. The motility phenotype in the L. Interestingly, hydin knockdown in C. Curling may represent the failure of flagellum bending to reverse during progression of the normal flagellum waveform down the flagellum, leaving the flagellum locked at one extreme of bending, analogous to the ciliary beat hydin phenotype.