After its internalisation by professional phagocytes, the first strategy of Mycobacterium tuberculosis and its close relative Mycobacterium marinum to escape the bactericidal phagosome is to impede its maturation and tailor the Mycobacterium-Containing Vacuole (MCV) as a permissive niche allowing the proliferation of the pathogen (Soldati and Neyrolles, 2012). From the very beginning, bacteria progressively gain access to the cytosol through the action of the ESX-1 secretion system, via the secretion of the membranolytic effector EsxA and the mycobacterial branched apolar lipids phthiocerol dimycocerosates (PDIMs)( Pym et al., 2002; Lerner et al., 2018; Quigley et al., 2017; Augenstreich et al., 2019; Lienard et al., 2020; Osman et al., 2020). The ESX-1 secretion system plays a crucial role for M. marinum virulence and intracellular growth, and is primarily encoded by the genes within the ‘region of difference 1’ (RD1) locus. M. marinum mutants with non-functional ESX-1 inflict significantly less MCV membrane damage and fail to become exposed to or escape to the cytosol, hampering their detection by the host cell-autonomous defence machineries (Cardenal-Muñoz et al., 2017; Gao et al., 2004). Once in contact with the cytosol, the wild-type (WT) bacteria within damaged MCVs are detected and tagged with signals that promote MCV damage repair as well as selective anti-bacterial autophagy, termed xenophagy (López-Jiménez et al., 2018). To complete the infection cycle, the pathogen must reach the cytosol and be released by host-cell lysis, exocytosis or ejection in order to disseminate to adjacent bystander cells (Hagedorn et al., 2009; Queval et al., 2017; Cardenal-Muñoz et al., 2017; López-Jiménez et al., 2018).

Xenophagy is fundamental for eukaryotic cell-autonomous immunity (Sharma et al., 2018; Deretic et al., 2013). It requires the coordinated action of about 15 autophagy-related genes (ATG) and is initiated by the recruitment of the core-autophagy factors Atg1 (ULK1 in mammals) kinase complex and Atg9 (ATG9 in mammals) to the nascent phagophore – a double membrane crescent-like structure. Its closure around the cargo depends on the Atg16-Atg12-Atg5 E3-like complex, and the lipidation of Atg8 (LC3 in mammals), which marks the phagophore (Mesquita et al., 2017). The resulting autophagosome fuses with lysosomes allowing the degradation of its content. Xenophagy requires detection and selective recruitment of the pathogen to the phagophore by means of autophagy cargo receptors such as p62 (SQSTM1 in mammals) that link ubiquitin-tagged bacteria and host components with Atg8 family proteins on the phagophore membranes, thereby enforcing proximity between the pathogen and the autophagosome (Boyle and Randow, 2013). Autophagy is involved in the removal of extensively damaged compartments by a specific macroautophagy termed lysophagy. Autophagy also cooperates with ESCRT to repair sterile- or pathogen-induced membrane damage (Skowyra et al., 2018; López-Jiménez et al., 2018; Papadopoulos et al., 2020). The ESCRT-III complex functions in membrane deformation away from the cytosol and plays a critical role in various membrane remodelling processes, including phagophore closure, autophagosome-lysosome fusion, plasma membrane, and lysosome membrane repair (Vietri et al., 2020; Schuck, 2020). One thoroughly studied ESCRT function is the coupling of cargo sorting and intralumenal vesicles formation required for degradation of receptors.

The endolysosomal and MCV membrane ruptures generate morphological and topological landscape for the detection machineries which deposit ‘repair-me’ and ‘eat-me’ signals (Boyle and Randow, 2013; Koerver et al., 2019; Papadopoulos et al., 2020). Ubiquitination is a well-studied, highly conserved and versatile post-translational modification used as a signalling platform in diverse catabolic processes and playing a role during infection with various intracellular bacteria. In mammalian cells, the RING domain E3 ligases LRSAM1 and TRAF6 have been shown to promote ubiquitination of vacuoles containing Salmonella Typhimurium and Chlamydia trachomatis bacteria, and the protozoan parasite Toxoplasma gondii (Huett et al., 2012; Haldar et al., 2015), and NEDD4 (Pei et al., 2017), Parkin (Manzanillo et al., 2013), Smurf1 (Franco et al., 2017) to mediate ubiquitination of mycobacteria and host proteins during infection. In addition, the mammalian cytosolic lectins, galectins, recognize damage by binding exposed glycans on the lumenal membrane leaflets and components of bacteria cell wall, thereby serving as ‘eat-me’ tags for autophagy. Moreover, complexes such as TRIM16-Galectin3 also mediate autophagy removal of damaged phagosomes and lysosomes during pathogen invasion (Chauhan et al., 2016; Randow and Youle, 2014). The human tumour necrosis factor receptor-associated factors (TRAF1-7) function in a number of biological processes such as innate and adaptive immunity and cell death as E3 ubiquitin ligases and scaffold proteins (Xie, 2013). TRAFs are composed of several domains: the N-terminal domain containing a RING motif (except TRAF1), a series of Zn-finger motifs that connect the N- and C-terminal regions and the C-terminal TRAF domain (except for TRAF7) subdivided in TRAF-N coiled-coil domain and TRAF-C domain comprised of seven to eight antiparallel β-strands (Bradley and Pober, 2001; Park, 2018; Joazeiro and Weissman, 2000). The RING domain and the Zn-finger motifs of TRAF6 are required for the E3 ligase activity and together with the dimeric E2-conjugating enzyme complex Ubc13-UeV1A, TRAF6 catalyses the generation of poly-Ub chains linked via the lysine K63 of Ub, in a homo- or hetero-oligomerisation-dependent manner with other TRAF members (Middleton et al., 2017). The RING domain is also important for dimerization of trimeric TRAF proteins allowing the formation of signalling networks (Das et al., 2022). The TRAF-N domain enables TRAF proteins homo- and hetero-oligomerisation that is also crucial for their E3 ligase activity. The TRAF-C domain allows interaction with receptor and adaptor proteins (Yin et al., 2010). Endomembrane ruptures on one hand permit the pathogen to gain access to the cytosol, but on the other hand to be detected. Then, together with the vacuole membrane remnants, bacteria are targeted to the autophagy machinery. Defects in endomembrane repair and lysophagy correlate with weakened cellular defences against pathogens, ageing, cancer and neurodegeneration (Papadopoulos and Meyer, 2017). Even though the role of ‘eat-me’ signals in autophagy is well understood, little is known about their implication in detection and repair of pathogen-induced or sterile membrane damage. Furthermore, how pathogen and membrane damages are detected, leading to the deposition of such ‘eat-me’ signals, remains unknown.

Using the social amoeba Dictyostelium discoideum – M. marinum model system for host-pathogen interactions, we have shown previously, that upon infection, M. marinum does colocalize with (Ub) and the autophagy markers Atg8 and p62, and that autophagy deficiency results in drastic increase in bacteria proliferation, and that failure to repair or recycle damaged MCVs results in increased cell death (Cardenal-Muñoz et al., 2017; Wang et al., 2018; Eriksson et al., 2020). Here, we have unravelled a novel function of a TRAF-like family protein RING domain-containing E3 ligase. Among half a dozen candidates explored, we found that the evolutionary conserved E3-ligase TrafE is recruited to MCVs or endolysosomes in a membrane damage- or tension-dependent manner. Importantly, we provide evidence that in the absence of TrafE, the autophagy restriction of M. marinum as well as the autophagy-mediated and ESCRT-mediated endolysosomal membrane damage repair are severely compromised, leading to precocious cell death.

In recent years, studies in mammals have revealed some of the components and the effector pathways that detect, repair and / or remove intracellular compartments disrupted by invading pathogens or by mechanical damage. Cells have developed molecular sensors that determine the size and the extent of membrane damage. Recent evidence indicate that small, pore-size damage is repaired by the ESCRT machinery, however extensive, and prolonged damage triggers the autophagy machinery. The latter appears to play both a repair as well as a remove role upon catastrophic damage. Despite intense research, we still need to extend our insight in the molecular factors involved in membrane damage detection and how it is translated into a vigorous and specific ubiquitination response. D. discoideum is a powerful model system to address the aforementioned questions thanks to its experimental versatility and the high evolutionary conservation of the ESCRT and the autophagy pathways with their mammalian counterparts.

It was previously shown that in D. discoideum, M. marinum infection or LLOMe-induced sterile damage leads to an increase of Ub- and Atg8-positive structures and to recruitment of the ESCRT subunits Tsg101, Vps32 and Vps4, reportedly ahead of the recruitment of autophagy markers p62 and Atg8 at the MCV and endolysosomes (Cardenal-Muñoz et al., 2017; López-Jiménez et al., 2018). In this study, we demonstrate that early after infection, the D. discoideum E3 ubiquitin ligase TrafE is recruited to MCVs in a membrane damage-dependent manner (Figures 1A, B,, 3A, B). This recruitment was significantly attenuated upon infection with M. marinum ∆RD1 (Figure 3A and B) that produces PDIMs but lacks a functional ESX-1 secretion system. We also demonstrate that the intracellular growth of M. marinum-lux is significantly increased in atg1-KO and trafE-KO cells compared to WT cells (Figure 2A), suggesting that xenophagy is the main M. marinum cell-autonomous restriction pathway. In addition, cells lacking the E3 ligase TrafE show exceptionally high and early susceptibility to infection with WT M. marinum which is not the case in the autophagy-deficient atg1-KO cells (Figure 2E). Upon starvation, atg1-KO cells that are fully defective in autophagy, display severe developmental phenotypes and do not proceed beyond aggregation (Otto et al., 2004). In contrast, trafE-KO cells successfully complete their developmental cycle and form spores (Figure 2—figure supplement 1A), emphasizing the functional specificity of TrafE to endolysosomal membrane damage. Altogether, our data indicate that trafE-KO phenocopies the autophagy-deficient atg1 mutants in terms of unrestricted M. marinum intracellular growth, however the higher cytotoxicity exerted by bacteria in trafE-KO cells compared to WT and atg1-KO cells (Figures 2E and 3D) leads to the speculation that TrafE might be upstream of both ESCRT- and autophagy-mediated membrane repair pathways. Following that hypothesis, the particularly rapid death of infected trafE-KO cells likely results from inefficient MCV repair, and leads to early bacteria escape and release by host cell lysis (Figure 2B and D, Figure 2—figure supplement 1B).

Ubiquitin is required for various aspects of autophagy, such as removal of protein aggregates (aggrephagy), recycling of mitochondria (mitophagy) and bacteria (xenophagy), or endolysosomal homeostasis (lysophagy). Xenophagy depends on decoration of intracellular pathogens with K63-linked Ub chains that bring bacteria to the phagophore membrane via autophagy cargo receptors such as p62 and NDP52. We demonstrated that although the levels of polyubiquitin-positive MCVs remain unaffected in M. marinum-infected trafE-KO cells, the levels of K63-linked polyUb-positive MCVs are significantly decreased but not abolished compared to wt D. discoideum cells (Figure 4A, B, C, D and ), possibly due to the presence of other E3-ligases, such as for instance TrafC, which is also recruited to MCVs during infection and might have partially redundant functions (Figure 1—figure supplement 3C). It has been shown that human TRAF6 forms heterodimers with TRAF2, TRAF3, and TRAF5 through their RING domains and that the resulting heterodimers are more stable than the TRAF6 homodimers (Das et al., 2021). Therefore, the severity of the trafE-KO phenotypes during infection may be due to the instability or non-functionality of a potential heterodimerization redundant partner(s), such as other D. discoideum TRAFs. Furthermore, we found that the recruitment of TrafE to MCVs is abolished in the absence of its RING domain and not when the TRAF domain is deleted (Figure 5A and B), likely because RING domains-mediated dimerization confers the specificity to the substrate via TrafE interaction with the E2-conjugating enzyme (Middleton et al., 2017; Kiss et al., 2021). Nevertheless, both domains are equally important for the restriction of M. marinum intracellular growth (Figure 5C).

Similar to xenophagy, lysophagy also depends on Ub and it has been shown that ubiquitination of Lysosome-Associated Membrane Protein 2 (LAMP2) in damaged lysosomes leads to their autophagic degradation (Papadopoulos et al., 2017). In addition, recent studies in mammalian cells have demonstrated that disrupted lysosomes leak protons and reactive oxygen species that lead to pyroptotic cell death (Papadopoulos et al., 2020). Repair of damaged lysosomes is vital for the cells and depends both on the ESCRT machinery and lysophagy, which repair and / or remove extensively damaged compartments (López-Jiménez et al., 2018; Daussy and Wodrich, 2020). Studies in HeLa Kyoto cells have demonstrated that membrane tension plays a role in endosomal membrane remodelling and that both hyperosmotic shock and LLOMe-induced perforations, result in a decrease of membrane tension sufficient to trigger the recruitment of the ESCRT-III subunit CHMP4B (Mercier et al., 2020). Remarkably, we found that TrafE is recruited to endolysosomes minutes after LLOMe treatment or hyperosmotic shock (Figures 6A, D, 7A and B), suggesting its involvement in endolysosomal membrane remodelling and repair signalling pathways. We also demonstrate that, unlike WT D. discoideum cells, trafE-KO cells fail to restore their endolysosomal pH after LLOMe-induced sterile damage (Figure 6G and H). Furthermore, as observed during M. marinum infection, trafE-KO mutant cells are extremely susceptible to LLOMe compared to atg1-KO or WT cells (Figure 7E), in agreement with our hypothesis that TrafE is upstream of ESCRT and autophagic membrane repair or removal pathways. Comparison of total RNA extracted from WT and trafE-KO cells under basal conditions indicated misregulation of nearly all genes belonging to the autophagy and the ESCRT families (Figure 8B), pointing to a connection between these pathways which TrafE may link.

Therefore, we set out to discern where ESCRT and autophagy intersect and importantly how TrafE may bridge the two pathways. As part of the cell survival mechanisms, autophagy is induced upon starvation to consume cytosolic constituents and to repair or remove extensively damaged compartments. As indicated by an increase of GFP-Atg8a puncta, we demonstrated that upon starvation autophagy is initiated in both WT and trafE-KO cells (Figure 9A and B). Therefore, the absence of TrafE does not affect autophagy initiation but rather its effectiveness as revealed by accumulation of GFP-Atg8a-positive structures in trafE-KO cells (Figure 9A and B). In a similar fashion, during sterile damage, despite the modest increase of GFP-Atg8a puncta in trafE-KO cells compared to WT (Figure 9C), these autophagosome-like compartments persisted (Figure 9D).

The ESCRT machinery has been extensively studied for its involvement in membrane remodelling, including regulation of autophagosome maturation (Takahashi et al., 2018; Zhou et al., 2019). In the present study, we show for the first time that in D. discoideum cells during starvation, the ESCRT accessory protein ALIX and ESCRT-III subunit Vps32 are recruited to dextran-negative compartments (Figure 10—figure supplement 1A, B) in contrast to starved atg1-KO cells (Figure 10—figure supplement 1C, D). To our surprise, compared to starved WT cells, absence of TrafE lead to a strong accumulation of ALIX-GFP and GFP-Vps32 while the number of GFP-Vps4 foci remained at its basal level (Figure 10—figure supplement 1E–G). Importantly, we showed that in trafE-KO cells, LLOMe causes significant build-up of ALIX-GFP or GFP-Vps32 structures relative to WT cells (Figure 10A, B, C and D), without concomitant and functionally crucial GFP-Vps4 recruitment (Figure 11A and B, Figure 11—figure supplement 1). Furthermore, in complemented trafE-KO cells, cytosolic GFP-Vps4 was redistributed to LLOMe-damaged compartments and colocalized with mRFP-TrafE (Figure 11C and D). Significantly, whilst in TrafE mutant cells the number ALIX-GFP structures was abnormal in mock- and LLOMe-treated cells, the K63-polyubiquitination of damaged compartments was severely reduced (Figure 12B, D and E). Altogether, these results demonstrate that in D. discoideum cells ESCRT and autophagy pathways intersect during endolysosomal membrane repair in which the absence of TrafE leads to striking functional disruptions of both machineries.

All data generated or analysed during this study are included in the manuscript and supporting files; Source data files have been provided for Figures 1B, 1C, 1D, 1E, 2A, 2B, 2C, 2D, 2E, 3B, 3C, 3D, 4C, 4E, 5B, 5C, 6D, 6F, 6H, 7B, 7D, 7E, 8A, 8B, 8C, 9B, 9C, 10C, 10D, 11B, 12D, 12E and for Figure 1 - figure supplement 3A, B, C, D, 4A, B, Figure 10 - supplement 1C, 1D, 1E, 1F, 1G. The graph from Figure 1 - figure supplement 2 was generated by analysis of publicly available data (Hanna et al., 2019). The MCV proteomics information was obtained from a publicly available dataset (Guého et al., 2019).

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Author details

1. Lyudmil Raykov

   Départment de Biochimie, Faculté des Sciences, University of Geneva, Geneva, Switzerland

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7989-610X

2. Manon Mottet

   Départment de Biochimie, Faculté des Sciences, University of Geneva, Geneva, Switzerland

   Contribution

   Formal analysis, Investigation, Visualization, Methodology

   Competing interests

   No competing interests declared

3. Jahn Nitschke

   Départment de Biochimie, Faculté des Sciences, University of Geneva, Geneva, Switzerland

   Contribution

   Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

4. Thierry Soldati

   Départment de Biochimie, Faculté des Sciences, University of Geneva, Geneva, Switzerland

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Project administration, Writing - review and editing

   For correspondence

   thierry.soldati@unige.ch

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2056-7931

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