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Supplementary Notes 1 2 Supplementary Note 1 1 Supplementary Notes 2 3 Supplementary Note 1. Functional characterization 4 Facial and gut microbiomes comparisons 5 We also identified 2 genes from lipid metabolism, 2 genes to glycan biosynthesis, and metabolism 6 and peptidoglycan biosynthesis, and 1 gene present only the face dataset related to 7 phenylpropanoid biosynthesis from Alistipes (related to protection from UV light, and defence 8 against herbivores and pathogens [1–3]). Interestingly, ~98x more bacteria in the face microbiome 9 is annotated as moderate halophilic (face= 11,239, gut= 115), as well as ~239 times more 10 psychrophilic bacteria in the face (face= 18,886, gut= 79). The top 5% with the largest difference 11 in abundance from the pathways that drive variation between the face and gut microbiomes, 12 contains the metabolism of fructose and mannose, starch and sucrose, galactose, and amino sugar 13 and nucleotide sugar, all of them more abundant in the gut microbiome. 14 15 Microbial cores 16 Besides the defined microbial taxonomic and functional cores obtained from the MGmapper 17 results (Additional File 11), we defined other types of cores based on the taxonomies assigned to 18 the annotated genes. The percentage of annotated genes in the face dataset has a median of 72.61% 19 (mean of 57.8%), and a median of the gut dataset is 66.75% (mean of 65.08%). From the nr gene 20 catalogue we defined 2 types of cores. A strict core, in which we keep those genes present in a 21 given minimum number of samples taking the taxa from where the genes derive into account 22 (Table S5). The second type of core, a relaxed one, does not take taxonomy of the genes into 23 account, and keeps those genes present in a given minimum number of samples (Table S6). 1 24 Looking at the taxonomic identifications from the protein annotations, we found 12 virus taxa in 25 all the face samples, 7 fungi, and 26 bacterial strains. In the gut samples, we found 9 bacterial 26 strains, 11 fungi, and 18 viruses. 27 28 Cadaverine and putrescine: Three of the main molecules produced in a decomposing body are 29 nitrate reductase (converting nitrite to ammonia) [4], cadaverine (lysine decarboxylase) [5], and 30 putrescine (ornithine decarboxylase) [5] (Additional File 5). In this regard, we identified in the 31 face MOCAT nr strict core a spermidine synthase gene from Janthinobacterium sp. HH01, and 32 spermidine/putrescine ABC transporter ATPase in both face and gut MOCAT strict cores from 33 Herbaspirillum sp. GW103. Sulphur compounds are also emitted by decomposing carcasses [6], 34 likely derived from methionine and cysteine degradation. This likely explains the identification of 35 the metabolism of cysteine and methionine as the two most abundant subclasses from the amino 36 acids metabolism in both face and gut microbiomes. A carcass also produces volatile organic 37 compounds [7], such as acetone, methyl ethyl ketone, toluene, ethylbenzene, m,p-xylene, styrene, 38 and o-xylene. In this regard, toluene degradation is one of the subclasses not driving variation in 39 the face functional intra samples comparison, and the MOCAT face cores have more genes related 40 to xenobiotics biodegradation metabolism than those of the gut microbiome (Additional File 5). 41 42 Supplementary Note 2. Microbiome cores identifications 43 Core microbiome identification: In the filtered MGmapper taxonomic profiling, we identified 44 1,483 species in the facial samples, 638 of which are in at least 50% of the samples (relaxed core), 45 and only 184 in at least 80% of the samples (strict core). In the gut microbiome we found 1,419 46 microbial species, with only 322 present in at least 50% of the samples, and 129 in at least 80%. 2 47 In the functional characterization we identified a total of 238,065 nr unique bacterial genes in the 48 face microbiome and 387,951 nr unique bacterial genes in the gut microbiome (Additional File 4, 49 Tables S4, S5). Besides the defined microbial taxonomic and functional cores obtained from the 50 MGmapper results (Additional File 11), we defined other types of cores based on the taxonomies 51 assigned to the annotated genes. The percentage of annotated genes in the face dataset has a median 52 of 72.61% (mean of 57.8%), and a median of the gut dataset is 66.75% (mean of 65.08%). From 53 the nr gene catalogue we defined 2 types of cores. A strict core, in which we keep those genes 54 present in a given minimum number of samples taking the taxa from where the genes derive into 55 account (Table S5). The second type of core, a relaxed one, does not take taxonomy of the genes 56 into account, and keeps those genes present in a given minimum number of samples (Table S6). 57 Looking at the taxonomic identifications from the protein annotations, we found 12 virus taxa in 58 all the face samples, 7 fungi, and 26 bacterial strains. In the gut samples we found 9 bacterial 59 strains, 11 fungi, and 18 viruses. 60 61 Supplementary Note 3. Digestive role of the gut microbiome 62 Intestinal microbiome related to digestion: Among the taxa present in higher abundance in the 63 face microbiome than in the gut microbiome, we identified taxa and functions that are usually part 64 of the gut microbiome of mammals (Additional File 3). These bacteria could be derived from the 65 carrion but be removed from the vulture gut microbiome. For example, present only in the face 66 dataset is Cellulophaga lytica, which is capable of degrading proteins and polysaccharides [8], as 67 well as Flavobacterium columnare, which produces gelatin-degrading and chondroitin sulfate- 68 degrading enzymes [9,10]. This is relevant given that chondroitin sulfate is one of the main 69 structural components of cartilage. Although we did not identify these genes from F. columnare, 3 70 we identified chondroitin sulfate ABC lyase genes in both face (4 genes from Bacteroides and 71 Proteus) and gut microbiomes (13 genes from Bacteroides, Edwardsiella, and Proteus). 72 73 Fusobacterium digestive roles: It has been proposed that the abundance of Fusobacterium in the 74 gut could aid in the digestion of meat, given their ability to metabolize amino acids [11,12]. This 75 suggestion is supported by the finding of F. nucleatum and F. varium in the vulture’s gut 76 microbiome. One of the most abundant genes in the gut microbiome is an alpha-2-macroglobulin 77 family protein from F. mortiferum (the most abundant Fusobacterium in the gut), this protein has 78 been suggested to be used in bacteria as a colonization rather than a virulence factor [13]. Besides, 79 eukaryotic alpha-2-macroglobulin, produced by the liver, binds to and removes MMP-2 and MMP- 80 9 (active forms of the gelatinase), which is produced in the stomach to digest gelatin [13,14]. 81 However, gelatin’s colloidal properties aid in the digestion of various types of food [15,16]. 82 Furthermore, bacterial alpha-2-macroglobulin can be structurally very similar to that of eukaryotes 83 [17]. This suggests that Fusobacterium could also be playing digestive aiding roles in the vulture 84 gut. 85 86 Supplementary Note 4. Taxonomic characterization 87 Pathogenic characterization: Looking at the identified bacteria taking into account the strain 88 information (Additional File 12), the maximum number of potentially pathogenic bacteria 89 identified in a sample (a face sample) was 482, and the minimum was 10, with a mean of 159.8. 90 Each pathogen was present in a mean number of 11.98, a minimum of 1, and a maximum of 75 91 (Clostridium perfringens ATCC 13124 and Clostridium perfringens str. 13). We found that the 92 face has more different species of potential pathogens than the gut (P= 0.036, face mean= 189.79, 4 93 gut mean= 137.29). Present in at least 90% of the samples are three Clostridium perfringens strains 94 which produce gas gangrene [18], and one Stenotrophomonas maltophilia, which produces 95 bacteremia, bronchitis, pneumonia, and urinary tract infection [19]. In the gut samples, the most 96 abundant hosts for the potentially pathogenic bacteria are human, chicken, turkey, cattle, pigs, and 97 mouse. For those in the face, the most abundant hosts are human, followed by cattle, and plants. 98 Among the 19 potentially pathogenic bacteria present only in the gut samples are Brachyspira 99 pilosicoli, Campylobacter coli and Campylobacter jejuni strains, some strains of C. difficile and 100 E. coli, Salmonella enterica strains, and some Shigellas (S. boydii, S. dysenteriae, and S. flexneri). 101 And among those 50 present only in the face dataset, we found various strains of Acinetobacter 102 baumannii, Actinobacillus pleuropneumoniae, Burkholderia, Capnocytophaga gingivalis ATCC 103 33624, some Vibrio species (V. harveyi HY01, V. ordalii ATCC 33509, V. shilonii AK1, V. 104 splendidus 12B01, and V. tasmaniensis ZS-17), various Xanthomonas, among others (Table 2). 105 106 Fusobacteria and Clostridia pathogenicity: It has been speculated that the large amount of 107 Fusobacteria and Clostridia in the vulture gut outcompetes other more virulent and toxic relatives, 108 being harmless pathogenic versions that occupy the space and resources that more pathogenic 109 versions would occupy otherwise, thus serving as a sort of probiotics [20]. To examine this 110 hypothesis, we searched for toxin-related genes from these taxa in the gut functional core. We 111 identified two putative enterotoxins from C. perfringes, and interestingly, also a protein in two gut 112 samples from the bacteriocinogenic plasmid pIP404 from C. perfringes [21]; less toxin-related 113 genes were found for Fusobacterium (Additional Files 9, 10).
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