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Encapsulins—Bacterial Protein Nanocompartments: Structure, Properties, and Application

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Encapsulins—Bacterial Protein Nanocompartments: Structure, Properties, and Application biomolecules Review Encapsulins—Bacterial Protein Nanocompartments: Structure, Properties, and Application Anna N. Gabashvili 1,2, Nelly S. Chmelyuk 1, Maria V. Efremova 3,4, Julia A. Malinovskaya 5, Alevtina S. Semkina 2 and Maxim A. Abakumov 1,2,* 1 Laboratory “Biomedical Nanomaterials”, National University of Science and Technology “MISiS”, Leninskiy Prospect, 4, 119049 Moscow, Russia; [email protected] (A.N.G.); [email protected] (N.S.C.) 2 Department of Medical Nanobiotechnoilogy, Pirogov Russian National Research Medical University, Ostrovityanova st, 1, 117997 Moscow, Russia; [email protected] 3 Department of Nuclear Medicine, TUM School of Medicine, Technical University of Munich, 81675 Munich, Germany; [email protected] 4 Institute of Biological and Medical Imaging and Institute of Developmental Genetics, Helmholtz Zentrum München, 85764 Neuherberg, Germany 5 D. Mendeleev University of Chemical Technology of Russia, 125047 Moscow, Russia; [email protected] * Correspondence: [email protected]; Tel.: +7-903-586-4777 Received: 29 April 2020; Accepted: 23 June 2020; Published: 26 June 2020 Abstract: Recently, a new class of prokaryotic compartments, collectively called encapsulins or protein nanocompartments, has been discovered. The shell proteins of these structures self-organize to form icosahedral compartments with a diameter of 25–42 nm, while one or more cargo proteins with various functions can be encapsulated in the nanocompartment. Non-native cargo proteins can be loaded into nanocompartments and the surface of the shells can be further functionalized, which allows for developing targeted drug delivery systems or using encapsulins as contrast agents for magnetic resonance imaging. Since the genes encoding encapsulins can be integrated into the cell genome, encapsulins are attractive for investigation in various scientific fields, including biomedicine and nanotechnology. Keywords: encapsulin; nanocompartment; cell labeling; MRI 1. Introduction The history of nanocompartments begins in 1994, when encapsulins were initially discovered as a high-molecular-weight complex in the bacterial culture supernatant of Brevibacterium linens, exhibiting bacteriostatic activity against various strains of Arthrobacter, Bacillus, Brevibacterium, Corynebacterium, and Listeria [1]. However, other encapsulins do not demonstrate such an effect, and even in the case of encapsulins from Brevibacterium linens in another study by Sutter et al., this fact was not confirmed [2,3]. Subsequently, homologous protein compartments were identified in the Mycobacterium tuberculosis [4] and Thermotoga maritima [5] culture supernatants. Moreover, these structures appeared to contain proteolytic enzymes. Encapsulins have also been identified during various studies in the bacteria Mycobacterium leprae, Streptomyces, and (much later) Quasibacillus thermotolerans [6–11]. In the mid-2000s, the observed high-molecular-weight aggregates were found to be protein capsid-like complexes [2,12,13]. The discovery of these structures spurred new research into prokaryotic nanocompartments. Some studies focused on the use of encapsulins as programmable nanoreactors or targeted delivery systems [14–21], while others investigated the physiological role of encapsulins and their cargo Biomolecules 2020, 10, 966; doi:10.3390/biom10060966 www.mdpi.com/journal/biomolecules Biomolecules 2020, 10, 966 2 of 12 Biomolecules 2020, 10, x 2 of 12 proteins in thethe nativenative bacterialbacterial context.context. BioinformaticBioinformatic analysis of sequenced genomes has revealed thousands of nanocompartment systems in both bacteria and archaea, with a wide variety of cargo proteins [[20,22–25].20,22–25]. 2. Structural Organization of the Shell Encapsulin shells are icosahedral (12 vertices,vertices, 20 faces, 30 edges) complexes formed by self-assembly of protomer proteins [[2,13,24].2,13,24]. Enca Encapsulinpsulin shell proteins are homologous to gp5-HK97 phage main capsid capsid protein protein (Figure (Figure 1A),1A), as as eviden evidencedced by by the the structural structural similarity similarity between between the thegp5 gp5protomer protomer protein protein and andencapsulin encapsulin shell shell protein protein [26]. [26 It]. should It should be noted be noted that that the theHK97 HK97 fold fold is iswidespread widespread in nature in nature and andhas hasbeen been observed observed in all inother all othertailed tailedphages phages [27], in [herpesvirus27], in herpesvirus capsids capsids[28], and [28 in], the and archaevirus in the archaevirus HSTV-1 HSTV-1[29]. Like [29 gp5,]. Like the gp5,encapsulin the encapsulin shell proteins shell proteins oligomerize oligomerize to form toa complete form a completenanocompartment. nanocompartment. As well as Asviral well caps asids, viral encapsulin capsids, shell encapsulin proteins shell can self-assemble proteins can self-assembleinto icosahedrons into icosahedrons of different ofsize diffs.erent For sizes.example, For example, encapsulins encapsulins from Pyrococcus from Pyrococcus furiosus furiosus and andMyxococcusMyxococcus xanthus xanthus consistconsist of 180 of 180 protomers protomers (30 (30-32‒32 nm nm in in diameter) diameter) (Figure (Figure 1C,D),1C,D), while those fromfrom Thermotoga maritima are composed of 60 protomers (24 nm inin diameter)diameter) (Figure1 1B)B)and andencapsulins encapsulins from Quasibacillus thermotolerans consist of 240 protomers (42 nm in diameter)diameter) [[2].2]. To To classify this structural organization,organization, a triangulationa triangulation number number can can be used. be used. The triangulationThe triangulation number number (T) is a virology(T) is a termvirology describing term describing the icosahedral the icosahedral packaging packaging of viral capsid of viral structural capsid structural elements elements and is the and quotient is the ofquotient dividing of dividing the number the ofnumber subunits of subunits in a capsid in a bycapsid 60 [30 by]. 60 Additionally, [30]. Additionally, T can be T can explained be explained as the numberas the number of subdivisions of subdivisions of each triangularof each triangular facet of icosahedronsfacet of icosahedrons into identical into equilateralidentical equilateral triangles. Thetriangles. number The of number these triangles of these is triangles equal to T.is Followingequal to T. this Following classification, this classification, the Pyrococcus the furiosus Pyrococcusand Myxococcusfuriosus andxanthus Myxococcusencapsulins xanthus formencapsulins icosahedrons form icosahedrons with T equal with to 3, QuasibacillusT equal to 3, thermotolerans Quasibacillus formsthermotolerans T = 4 icosahedrons, forms T = 4 andicosahedrons,Thermotoga and maritima Thermotogaforms maritima T = 1 icosahedron. forms T = The1 icosahedron. structure of The an encapsulinstructure of shell an encapsulin protomer protein, shell protomer like HK97 pr phageotein, gp5like protomer,HK97 phage has threegp5 protomer, conserved has domains: three aconserved peripheral domains: domain a (P), peripheral an axial domain domain (P), (A), an and axial an elongateddomain (A), loop and (E) an [2 ,elongated6,14,30,31 ].loop While (E) the[2,6,14,30,31].Pyrococcus While furiosus theand PyrococcusMyxococcus furiosus xanthus andencapsulin Myxococcus protomer xanthus encapsulin structures matchprotomer the HK97structures gp5 protomermatch the structure HK97 gp5 well protomer [13,24], onlystructure the A well and E[13,24], domains only from the the A Thermotogaand E domains maritima fromencapsulin the Thermotoga align wellmaritima with encapsulin those of the alignPyrococcus well furiosuswith thoseand Myxococcus of the Pyrococcus xanthus encapsulinfuriosus and protomer Myxococcus structures xanthus [2]. Inencapsulin particular, protomer the E loop structures from Thermotoga [2]. In particular, maritima theis E shorter loop from and Thermotoga rotated relative maritima to theis shorter E loops and of HK97rotated phage, relativePyrococcus to the E loops furiosus of, andHK97Myxococcus phage, Pyrococcus xanthus [furiosus2]. This, and allows Myxococcus the E loop xanthus to form [2]. a betaThis sheetallows with the theE loop E loop to form of a neighboringa beta sheet with protomer, the E creatingloop of a a neighboring tight interaction protomer, [2]. This creating may explaina tight whyinteraction the Thermotoga [2]. This may maritima explainencapsulin why the Thermotoga forms a T maritima= 1 capsid, encapsulin while the formsPyrococcus a T = 1 capsid, furiosus whileand Myxococcusthe Pyrococcus xanthus furiosusnanocompartments and Myxococcus xanthus can form nanocompartments a larger T = 3 capsid. can form a larger T = 3 capsid. Figure 1. Structural comparison of the capsomers/monomers and assembled capsid/encapsulins: Figure 1. Structural comparison of the capsomers/monomers and assembled capsid/encapsulins: (A) (A) HK97 phage, (B) Thermotoga maritima encapsulin, (C) Myxococcus xanthus encapsulin, HK97 phage, (B) Thermotoga maritima encapsulin, (C) Myxococcus xanthus encapsulin, (D) Pyrococcus (D) Pyrococcus furiosus encapsulin. (PDB-ID: 2FT1, 3DKT, 4PT2, and 2E0Z, respectively). furiosus encapsulin. (PDB-ID: 2FT1, 3DKT, 4PT2, and 2E0Z, respectively). It has been proposed that encapsulins and certain phage capsids have a common evolutionary originIt [has2,32 been]. This proposed hypothesis that is encapsulins supported by and the certain identification phage capsids of genes have encoding a common phage-like
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