Aegerolysins: Comparison
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Aegerolysins are remarkable proteins. They are distributed over the tree of life, being relatively widespread in fungi and bacteria, but also present in some insects, plants, protozoa, and viruses. Their function, in particular, is intriguing. Aegerolysin proteins are involved in various interactions by recognizing a molecular receptor in the target organism. Despite their abundance in cells of certain developmental stages and their presence in secretomes, only a few aegerolysins have been studied in detail. Formation of pores with various larger non-aegerolysin-like protein partners is one of the possible responses of the aegerolysin-producing organism in competitive exclusion of other organisms from the ecological niche.

  • aegerolysins
  • bacteria
  • fungi
  • insecticidal
  • lipid binding
  • lifestyle
  • membrane-attack complex/perforin domain (MACPF)
  • pore forming proteins

1. Introduction

The aegerolysin family (Pfam 06355) is a lesser-known protein family that has received increasing attention in recent years. The aegerolysin family consists of proteins that are biochemically characterized as β-structured proteins and share some common features: similar small molecular weights (15–20 kDa), low isoelectric points, and stability in a wide pH range [1]. Because they are non-core proteins, without a member of this protein family in each of the sequenced fungi, their distribution among fungal species is inconsistent, and different numbers of homologs have been reported for species within the same genus [2,3,4][2][3][4]. They are not only relatively widespread in fungi and bacteria, but also identified in few plants, protozoa, viruses, and insects [1,2][1][2].
In recent years, several reviews of this protein family have been published, but none of them included data on the ecology of the organisms producing them. In particular, their function is enigmatic, although some authors suggest a role in the development of the organism [1,2,3][1][2][3]. However, some of them function as two-component cytolysins that exhibit membrane permeabilization activity together with another non-aegerolysin-like protein [2,5][2][5]; these act together to perforate natural and artificial lipid membranes [1,2,5][1][2][5]. The aegerolysin-like proteins provide membrane lipid selectivity and recruit partner protein molecules to form a pore complex inserted into the membrane [2,5][2][5].
Despite the limited scientific knowledge about the function of aegerolysins, several potential applications are already emerging. Most commonly, some fungal aegerolysins serve as probes for the detection, labeling, and imaging of specific membrane lipids, lipid rafts, cancer cells, invertebrates, or parasites [4,6,7,8,9,10,11][4][6][7][8][9][10][11]. In high concentrations, they can induce both artificial lipid vesicles as well as live cells, such as blood cells or neuroblastoma cells, to bend and bud [10]. A role of some aegerolysins in combating obesity and related metabolic disorders has been recognized [10]. Their genes and expression may serve as markers for the progression of fruiting body differentiation during mushrooms cultivation [10] or as biomarkers to detect fungal exposure and progression of infectious disease [3,4][3][4]. In addition, antibodies produced against aegerolysins can serve as immuno-diagnostic tools [4]. Due to their variable sequence, aegerolysins serve as tools to identify of fungal phytopathogen isolates compared to some closely related species where the internal transcribed spacer barcoding method has failed [4]. Strong promoters regulating aegerolysin genes can promote the secretion of heterologous proteins from fungi in concomitant multi-gene expression [4]. Certain aegerolysins that combine with larger protein partners to form pore-forming complexes can be used to selectively eliminate insect pests [4,10][4][10] or to treat certain types of cancer cells [4,10][4][10].

2. Aegerolysins

WResearchers have collected (experimental) published data on 23 different aegerolysins and their variants. In total, they were characterized from 18 different species belonging to different kingdoms of tree of life. Twelve of these aegerolysins belong to fungi, four to bacteria, and one to insects and viruses. In fungi, they were characterized from four mushrooms (Agaricomycotina) from the order Agaricales: Pleurotus ostreatus, P. eryngii, Agrocybe aegerita, and Moniliophthora pernicious, as well as in the ordo Polyporales: Lignosus rhinocerotis (Table 1). The origin of these aegerolysins were also four filamentous Eurotimycetes from the ordo Eurotiales: Aspergillus fumigatus, A. niger, A. terreus, and A. oryzae (Table 1). Two species belonged to the Sordariomycetes, ordo Hypocreales: Beauveria bassiana, and Trichoderma atroviride, and another to the Dothideomycetes, ordo Pleosporales: Alternaria geisen (Table 1). There were four bacterial species, two belonging to Firmicutes: Bacillus thuringiensis and Clostridium bifermentans, and another two to Proteobacteria: Pseudomonas aeruginosa and Alcaligenes faecalis (Table 1). Another species belongs to Insecta—Lepidoptera, Noctuidae: Pseudoplusia includes, and another to Varidnaviria, Ascoviridae: Trichoplusia ni ascovirus 2c (Table 1).
Table 1.
 Organisms that contain aegerolysins according to taxonomy and lifestyles.
Organism Name Other Names Taxonomy Lifestyle/Niche Reference
    Fungi    
Pleurotus ostreatus Oyster mushroom

Hiratake		 Agaricomycotina

Agaricales Saprotroph

White rot

Nematocidal		 [15][12]
52]. Similar cytolytic effects were observed when PlyB was combined with other Pleurotus-derived aegerolysins, e.g., OlyA6, PlyA2 and EryA [78][53]. These heteromeric aegerolysin-based cytolytic complexes have been exploited as potent biopesticides for specific pests, with Cry16Aa/Cry17Aa/Cbm17.1/Cbm17.2 acting against Aedes mosquitoes, and Cry34Ab1/Cry35Ab1, AflP-1A/AflP-1B, OlyA6/PlyB, PlyA/PlyB, PlyA2/PlyB, or EryA/PlyB acting against Coleoptera species, especially the western corn rootworm.
Unexpectedly, partner proteins can be classified into five groups (Table 2, Figure 2): (1) PlyB and EryB have a similar MACPF fold; (2) the remaining models, including BlyB, showed a reasonably good superposition; BlyB has been shown to best align the structure of bacterial GNIP1Aa, another MACPF domain-containing protein [52,121][54][55]; (3) the Cry35Ab1 structure and (4) the AfIP-1B model do not superimpose with the PlyB structure or with each other; for AfIP-1B, the MACPF domain was found to be insignificant [52][54]; (5) Cry16Aa and Cry17Aa only superimpose with each other.
Table 2.
 List of published aegerolysins.
Short Name Aegerolysin/

Structure		 Membrane

Receptor		 Function Partner Protein Short Name Partner Protein/

Structure		 Organism Reference
PlyA Pleurotolysin A

PDB ID: 4OEBA		 SM/Chol n.d. PlyB Pleurotolysin B

PDB ID: 4OEJ

Membrane embedded PlyA/PlyB pore

PDB ID: 4V2T		 Pleurotus ostreatus [59,61][56][57]
Pleurotus eryngii King oyster or trumpet or brown mushroom

Boletus of the steppes

OlyAFrench horn mushroom

Aliʻi oyster		 Agaricomycotina

Agaricales Ostreolysin A SM/Chol

CPE/Chol

Lipid raftsSaprotroph

Grassland-litter decomposer

Facultatively biotrophic

Nematocidal		 [ Involvement in mushroom fruiting

Anticancer (+PlyB)		16][13]
PlyB Pleurotolysin B

PDB ID:

4OEJ Pleurotus ostreatus [63,64,65,66,67,68,69,[58][59][6070,]71,][65][76,[61]80,[62]84,[63]66][67 Cyclocybe aegerita Agrocybe aegerita

Poplar mushroom

Tea tree mushroom

Cha shu gu

Yanagi-matsutake

Sword-belt mushroom

Velvet pioppini		 Agaricomycotina

Agaricales Saprotroph

Weak white rot on hardwoods

Facultatively pathogenic		 [17][14]
[53][68][74][75][76][77][78][79][80][81][82] Moniliophthora perniciosa Crinipellis perniciosa

Witches’ broom disease		 Agaricomycotina

Agaricales Hemibiotrophic plant pathogen

Broad range of host
rOly Recombinant ostreolysin Lipid rafts? Antiproliferative

Pro-apoptotic		[18][15]
n.d. n.d. Pleurotus ostreatus [88,89,90][83][84][85] Lignosus rhinocerotis
PlyA2Tiger milk mushroom Agaricomycotina

Polyporales Pe.PlyA/Pleurotolysin A2Saprotroph SM/Chol

CPE/Chol

CPE



White rot		 Lipid rafts[19][16]
Insecticidal

(+PlyB) EryB Erylysin B Pleurotus eryngii [15,79,80,93,94,95,96][12][68][78][86][87][88][89] Neosartorya fumigata Aspergillus fumigatus Eurotimycetes

Eurotiales Saprotroph

Ubiquitous in soil and compost

Human (opportunistic) pathogen		 [20,21,22,23][17][18][19][20]
EryA Erylysin A CPE/Chol

CL/DPPC/Chol		 Insecticidal (+PlyB)

Inhibition of cytokinesis		 No No Pleurotus eryngii [78,80,][53][96,68][98,89][90]99[91] Aspergillus niger   Eurotimycetes

Eurotiales Saprotroph

Ubiquitous in soil and compost

Human opportunistic pathogen		 [
Aa-Pri1 Aegerolysin Aa-Pri120 n.d.,21,24,25,  26,27][17][18][21][22][23][24]
No No Agrocybe aegerita [63,100][58][92] Aspergillus terreus   Eurotimycetes

Eurotiales Saprotroph

Human opportunistic pathogen		 [20,21,28][17]
MpPRIA1[18][25]
Putative aegerolysin n.d.   MpPLYB? n.d. Moniliophthora perniciosa [101][93]
MpPRIA2 Putative aegerolysin n.d.   MpPLYB? n.d. Moniliophthora perniciosa [101][93] ,34,35][29][30][31][32]
Alternaria geisen Black spot of Japanese pear Dothideomycetes

Pleosporales Plant pathogen [36,37][33][34]
    Bacteria    
Bacillus thuringiensis   Firmicutes Ubiquitous opportunistic pathogen on vertebrates, plants, insects, nematodes, mollusks, protozoan, animal, and human parasites.

Soils, grain dusts, dead insects, water

Aerobic and spore-forming		 [38,39][35][36]
]85,[86,102,64[68][69][70][71]104][72][73]
OlyA6 Ostreolysin A6

PDB ID: 6MYJ		 SM/Chol

CPE/Chol

CAEP/POPC/Chol

Lipid rafts		 Insecticidal (+PlyB) PlyB Pleurotolysin B

PDB ID:

4OEJ		 Pleurotus ostreatus [72,73,74,75,78,79,80,81,82,83,87] Aspergillus oryzae   Eurotimycetes

Eurotiales Saprotroph [20,21,29][17][18][26]
Beauveria bassiana   Sordariomycetes

Hypocreales Entomopathogen

Endophyte

Soil and insects		 [30
GME7309,31][27][ GME7309_g aegerolysin-domain-containing protein28]
n.d.   n.d. n.d. Lignosus rhinocerotis [105][94] Hypocrea atroviridis Trichoderma atroviride Sordariomycetes

Hypocreales Mycoparasitic (including oomycetes)

Cosmopolitan, soil		 [32
Asp-HS Asp-hemolysin, Oxidized low-density lipoproteins Cytotoxic effects on murine macrophages and vascular endothelial cells

Induce cytokine genes		33 Asp-HSB n.d. Aspergillus fumigatus [107,108,109,110,111,112,113,114,115][95][96][97][98][99][100][101][102][103]
Asp-HS-like Asp hemolysin-like n.d. n.d. No No Aspergillus

fumigatus [114][102]
NigA1 Nigerolysin A1 n.d. n.d. No No Aspergillus niger [91,92][104][105]
NigA2 Nigerolysin A2 CPE/Chol n.d. NigB1 Nigerolysin B1 Aspergillus niger [91,92][104][105 Paraclostridium bifermentans

subsp. malaysia Clostridium bifermentans

subsp. malaysia Firmicutes Anaerobic, forming endospores

Mosquito larvicidal		 [40][37]
]
Ter Terrelysin n.d. n.d. No No Aspergillus terreus [28,116,117][25][106][107] Alcaligenes faecalis   Proteobacteria Soil, water, environments associated with humans

Human opportunistic pathogen

Nematocidal		 [41
AoHlyA Aspergillus oryzae hemolysin n.d.][ n.d.38]
No No Aspergillus oryzae [118,119,120][108][109][110] Pseudomonas aeruginosa   Proteobacteria Ubiquitous opportunistic pathogen on:

BlyAhumans, vertebrates, plants, and insects Beauveriolysin A[ SM/Chol

CPE/Chol		42 n.d., BlyB43,44,45,46][39][40][41][42][43]
Beauveriolysin B Beauveria bassiana [52][54]     Insecta    
Agl1 Trichoderma atroviride aegerolysin Conidiation

Antagonism		 n.d. No No Trichoderma atroviride [128][111] Chrysodeixis includens Pseudoplusia includes Lepidoptera

Noctuidae Plant pest (defoliator)

Larvae feed on a wide range of plants		 [
L152 Alternaria geisen aegerolysin n.d.47,48][44] n.d.[45]
L152B n.d. Alternaria geisen     Viria    
Trichoplusia ni ascovirus 6a1 Trichoplusia ni ascovirus 2c Varidnaviria

Ascoviridae Obligate pathogen

Pseudoplusia includens moth larvae [47,49,44][46]50,[47]51][[48]

3. Aegerolysin Binary Partner Proteins

Binary and quaternary cytolytic complexes of bacterial origin in which aegerolysin-like proteins are combined with larger, non-aegerolysin-like protein partner(s), described to date, include: Cry16Aa/Cry17Aa/Cbm17.1/Cbm17.2 from C. bifermentas subsp. malaysia [40][37]; Cry34Ab1/Cry35Ab1 from B. thuringiensis [130,134][49][50]; and AflP-1A/AflP-1B from A. faecalis [143][51]. In fungus P. ostreatus, PlyA forms a pore embedded in the membrane together with PlyB (Figure 1) [60][
[
36
]
[
33
]
Cry34Ab1


(Gpp34Ab1)
13.6 kDa Insecticidal crystal protein


PDB ID: 4JOX
Unknown protein receptor
Insecticidal


(+Cry34Ab1) Cry35Ab1

(Tpp35Ab1) 43.8 kDa insecticidal crystal protein

PDB ID: 4JP0		 Bacillus thuringiensis [39,129,130,131,132,133,134,135,136][36][49][50][112][113][114][115][116][117]
Cbm17.1 Hemolysin-like protein Cbm17.1 n.d. Insecticidal

(+Cry16Aa/Cry17Aa/

Cbm17.2)		 Cry16Aa, Cry17Aa, Cbm17.2 Pesticidal crystal-like protein Cry16Aa and Cry17Aa, Hemolysin-like protein Cbm17.2 Clostridium bifermentans [40,140,142][37][118][119]
Cbm17.2 Hemolysin-like protein Cbm17.2 n.d. Insecticidal

(+Cry16Aa/Cry17Aa/

Cbm17.1)		 Cry16Aa, Cry17Aa, Cbm17.2 Pesticidal crystal-like protein Cry16Aa and Cry17Aa, Hemolysin-like protein Cbm17.1 Clostridium bifermentans [40,140,142][37][118][119]
AfIP-1A Two-component insecticidal protein 16 kDa unit

PDB ID: 5V3S		 Unknown protein receptor

AfIP-1A/AfIP-1B membrane pore		 n.d. AfIP-1B Two-component insecticidal protein

77 kDa unit		 Alcaligenes faecalis [143,144][51][120]
RahU RahU protein

PDB ID: 6ZC1		 CPE/Chol n.d. No No Pseudomonas aeruginosa [145,148][121][122]
P23 n.d. n.d. n.d. No No Pseudoplusia includes [48][45]
TnAV2cgp029 n.d. n.d. n.d. No No Trichoplusia ni ascovirus 2c [49,50,149,150,152][46][47][123][124][125]
CL, cardiolipin; CAEP, ceramide aminoethylphosphonate; CPE, ceramide phosphoethanolamine; Chol, cholesterol; DPPC, dipalmitoylphosphatidylcholine; n.d., no data; ?, not enough data; PDB ID, Protein Data Bank identification code; POPC, phosphatidylcholine; SM, sphingomyelin.

Proteins containing a membrane-attack complex/perforin (MACPF) domain are transmembrane pore-forming proteins important for both human immunity and pathogen virulence. Little is known about the function of MACPF-like domain proteins in filamentous fungi and their taxonomic distribution. The number of putative MACPF proteins in a single fungal species ranges from zero to ten or more [155][126]. The identification and annotation of putative MACPF-like proteins is generally more error-prone because these genes have a higher number of introns [155][126]. The sequences can be divided into two groups. The proteins in the first group, such as PlyB or EryB, were assigned to the MACPF domain PF01823, which was confirmed by the 13-amino acid signature Y/F-G-X2-F/Y-X6-G-G typical of this domain, and they are grouped with human perforin. The second group of sequences is not recognized by the Pfam tool but still contains the typical MACPF/CDC signature, such as BlyB [155][126]. Fungal MACPF proteins probably contribute to various specific processes. While some of them were found in secretomes (without a typical signal sequence being recognized), others are intracellular, and some of them might be involved in pathogenesis, although probably not all [155][126]. The large number of introns, the sporadic taxonomic distribution, and the different number of MACPF proteins per fungal species might indicate the involvement of horizontal gene transfer mechanisms in specific ecological niches [155][126]. Putative MACPF-like domains were identified in the genomes of fungal species with different lifestyles; some of them are pathogenic, such as plant pathogen M. perniciosa, the caterpillar fungus C. militaris, or the nematode trap fungus Arthrobotrys oligospora. Some of the species are also saprophytic, such as the white rot fungus P. ostreatus, grassland-litter decomposers P. eryngii, saprophytic and food-producing A. oryzae, or saprophytic soil fungus A. nidulans [155][126].
However, the binary protein partner Cry35Ab1 does not have a MACPF domain associated with it. Instead, it contains the C-terminal domain toxin 10 (PF05431), which is typical of a family of insecticidal crystal toxins of Bacillus, named after the insecticidal crystal toxin P42. Cry35Ab1 also has an additional N-terminal ricin-type β-trefoil lectin domain (PF00652) (classified as insignificant only) [52,130][49][54].
Cry16Aa and Cry17Aa are delta endotoxins composed of three distinct structural domains, endotoxin N, M, and C, respectively. An N-terminal helical bundle domain is involved in membrane insertion and pore formation (PF03945), a central β-sheet domain is involved in receptor binding (PF00555), and the C-terminal β-sandwich domain interacts with the N-terminal domain to form a channel (PF03944). During sporulation, the bacteria produce crystals of delta endotoxins. When an insect ingests these proteins, they are activated by proteolytic cleavage. For all such proteins, the N-terminus is cleaved, and for some members, a C-terminal extension is also cleaved. After activation, the endotoxin binds to the intestinal epithelium and, by the forming cation-selective channels, causes cell lysis, which leads to death [137,156][127][128].
Surprisingly, it was observed in the genome of P. ostreatus that the two genes encoding the pair of pore-forming proteins also form a bidirectional pair with 5′–5′ orientation of plyA (priA) and plyB [91,92][104][105]. Similar gene pairs encoding putative bicomponent toxins have been observed previously, such as Asp-HS with Asp-HSB, NigA2 with NigB1, and BlyA with BlyB from A. fumigatus, A. niger, and B. bassiana, respectively [52,92][54][105]. Moreover, such gene pairs have been also identified in other entomopathogenic fungi besides in B. bassiana, in the genomes of Cordiceps militaris, Metarizium acridum, M. anisopliae, M. robertsii, and Ophiocordiceps sinensis, but the involvement of these protein pairs in pore formation remains to be confirmed [52][54]. Here, wresearchers identified two additional putative pairs:  PlyA2 with EryB from P. eryngii and L152 with L152B from A. geisen (Figure 31). The gene locations of the aegerolysin and putative MACPF-like genes in the genomes of some fungi and bacteria are schematically shown in Figure 31. A total of six fungal (putative) bicomponent toxins form a bidirectional gene pair with 5′–5′ orientation of the adjacent gene, and distances between the two genes vary (Figure 31). Clusters of genes encoding fungal secondary metabolites may also contain some reverse-oriented genes that may nevertheless show coordinate expression. In contrast to the fungal gene pairs, the AfIP-1A/AfIP-1B gene pair encoded on the bacterial chromosome has the same sense orientation (Figure 31). The bicomponent toxin gene pair Cry34Ab1/Cry34Ab1 is known to be plasmid-encoded, but the variation of the plasmid in the bacterium B. thuringiensis is exceptionally high to see if these two genes are adjacent. The Cry operon in plasmid pCryO of C. bifermentans subsp. malaysia contains four genes downstream of the promoter pCyt: Cry16Aa is located 91 base pairs (bp) downstream, followed by Cry17Aa, which is located 426 bp downstream, followed by Cbm17.1, and 1022 bp downstream, followed by Cbm17.2 [40][37]. Their placement at the same locus or under the control of the same promoter does not necessarily lead to their joint action, but rather indicates coordinated expression.
Toxins 14 00629 g003 550
Figure 31. Aegerolysin gene loci in fungal and bacterial genomes. Grey arrows, aegerolysin genes; Cian arrows, membrane-attack-complex/perforin (MACPF)-like genes; plyA (priA) aegerolysin with plyB, pleurotolysin B gene from Pleurotus ostreatus PC9 whole genome sequence; [53][129]; PlyA2 with EryB from P. eryngii ATCC 907,970 [157][130]; Asp-HS with Asp-HSB from Neosartorya fumigata (Aspergilus fumigatus) Af293 [22][19]; nigA2 with nigB1, nigerolysin A2, and B1 gene A. niger CBS 513.88 [27][24]; blyA and blyB, beauveriolysin A and B gene from Beauveria bassiana ARSEF 2860 [158][131], L152 with L152B from Alternaria geisen BMP2338 [159][132], and AfIP-1A with AfIP-1B from Alcaligenes faecalis GCA_003521065; numbers, size of genes, and distance among genes in base pairs. Gene sizes and distances are scaled.
Some of the aegerolysins included in this revisewarch are also encoded in genomes that do not have an adjacent (MACPF domain-containing) partner protein; such aegerolysins are the fungal  EryA, Aa-Pri1, Asp-HS-like, Ter, AoHlyA, and NigA1, bacterial RahU, insects P23 and the ascoviral TnAV2c gp029 (Table 2). For some of them, insufficient data are available, such as for the MpPRIA1, MpPRIA2, and MpPRIB, because the sequenced countings are too short, or no genomic data were found for GME7309 (Table 2). However, a combined action with MACPF domain-containing proteins encoded elsewhere in the genome cannot be excluded, as some aegerolysins, such as PlyA2 and EryA from P. eryngii, have been shown to exhibit cytolytic activity when combined with their non-native partner with component B, PlyB, from P. osteratus [78][53].

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