Five novel bifidobacterial species isolated from faeces of primates in two Czech zoos: Bifidobacterium erythrocebi sp. nov., Bifidobacterium moraviense sp. nov., Bifidobacterium oedipodis sp. nov., Bifidobacterium olomucense sp. nov. and Bifidobacterium panos sp. nov.

Abstract

Five Bifidobacterium strains, VB23T, VB24T, VB25T, VB26T and VB31T, were isolated from chimpanzee (Pan troglodytes), cotton-top tamarin (Saguinus oedipus), Goeldi’s marmoset (Callimico goeldii), moustached tamarin (Saguinus mystax) and patas monkey (Erythrocebus patas), respectively, which were kept in two Czech zoos. These strains were isolated from faecal samples and were Gram-positive, non-motile, non-sporulating, anaerobic and fructose-6-phosphate phosphoketolase-positive. Phylogenetic analyses based on 16S rRNA revealed close relatedness between VB23T and Bifidobacterium angulatum LMG 11039T (96.0 %), VB24T and Bifidobacterium pullorum subsp. pullorum DSM 20433T (96.1 %), VB25T and Bifidobacterium goeldii LMG 30939T (96.5 %), VB26T and Bifidobacterium imperatoris LMG 30297T (98.1 %), and VB31T and B . angulatum LMG 11039T (99.40 %). Internal transcribed spacer profiling revealed that VB23T, VB24T, VB25T, VB26T and VB31T had highest similarity to Bifidobacterium breve LMG 13208T (77.2 %), Bifidobacterium longum subsp. infantis ATCC 15697T (85.8 %), Bifidobacterium biavatii DSM 23969T (76.9 %), B. breve LMG 13208T (81.2 %) and B. angulatum LMG 11039T (88.2 %), respectively. Average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) analyses with their closest neighbours supported the independent phylogenetic positions of the strains with values between 86.3 and 94.3 % for ANI and 25.8 and 54.9 % for dDDH. These genomic and phylogenetic analyses suggested that the evaluated strains were novel Bifidobacterium species named Bifidobacterium erythrocebi sp. nov. (VB31T=DSM 109960T=CCUG 73843T), Bifidobacterium moraviense sp. nov. (VB25T=DSM 109958T=CCUG 73842T), Bifidobacterium oedipodis sp. nov. (VB24T=DSM 109957T=CCUG 73932T), Bifidobacterium olomucense sp. nov. (VB26T=DSM 109959T=CCUG 73845T) and Bifidobacterium panos sp. nov. (VB23T=DSM 109963T=CCUG 73840T).

The genus Bifidobacterium: from genomics to functionality of an important component of the mammalian gut microbiota

“…Taxonomically classified as members of the Bifidobacteriaceae family, bifidobacteria are Gram-positive, non-motile, non-spore forming, anaerobic, saccharolytic microorganisms with a Y-shaped or ‘bifid’ morphology, and a high G + C DNA content [18] . Starting from the description of the first bifidobacterial species, isolated by Tissier in 1899 from the fecal sample of a breast-fed infant [19] , the number of species belonging to the genus Bifidobacterium has increased over time with several species being identified only recently, including Bifidobacterium erythrocebi , Bifidobacterium moraviense , Bifidobacterium oedipodis , Bifidobacterium olomucense , Bifidobacterium panos , Bifidobacterium cebidarum , Bifidobacterium leontopitheci , Bifidobacterium saimiriisciurei and Bifidobacterium platyrrhinorum , all isolated from the feces of various monkey species [20] , [21] , [22] , and Bifidobacterium canis and Bifidobacterium choloepi , isolated from the feces of a dog and sloth, respectively [23] , [24] . The genus Bifidobacterium represents the deepest branching lineage within the phylum Actinobacteria, and currently comprises 94 recognized (sub)species [22] , [25] .…”

Genetic insights into the dark matter of the mammalian gut microbiota through targeted genome reconstruction

“…In order to discover putative novel bifidobacterial species, faecal material of non‐human primates was selected as an appropriate source since it had recently been shown to represent an important reservoir of bifidobacterial diversity (Duranti et al ., 2017 ; Lugli et al ., 2018b ; Modesto et al ., 2018a ; Modesto et al ., 2018c ; Modesto et al ., 2018b ; Duranti et al ., 2019 ; Modesto et al ., 2019a ; Duranti et al ., 2020 ; Modesto et al ., 2020a ; Neuzil‐Bunesova et al ., 2021 ). Consequently, the examined samples were selected based on a previous study investigating the co‐phylogeny of primate‐associated bifidobacteria (Lugli et al ., 2020b ).…”

“…Among microorganisms that reside in the animal gut, members of the genus Bifidobacterium represent an important and extensively studied bacterial component due to the generally accepted important role they play as part of the early gut microbiota during the very first stages of life of mammals (O'Callaghan and van Sinderen, 2016 ; Turroni et al ., 2018 ; Mancabelli et al ., 2020 ; Turroni et al ., 2020 ). In the last 3 years, a large number of novel species of the genus Bifidobacterium have been described, resulting in a genus that currently constitutes 94 different (sub)species (Duranti et al ., 2017 ; Lugli et al ., 2018b ; Modesto et al ., 2018a ; Modesto et al ., 2018c ; Modesto et al ., 2018b ; Duranti et al ., 2019 ; Modesto et al ., 2019b ; Modesto et al ., 2019a ; Duranti et al ., 2020 ; Modesto et al ., 2020b ; Modesto et al ., 2020a ; Neuzil‐Bunesova et al ., 2020 ; Neuzil‐Bunesova et al ., 2021 ). The majority of these most recently discovered novel bifidobacterial species have been isolated from mammals, in particular from faecal samples of primates, such as species of the genus Callimico , Callithrix , Saguinus and Saimiri (Duranti et al ., 2017 ; Lugli et al ., 2018b ; Modesto et al ., 2018a ; Modesto et al ., 2018c ; Modesto et al ., 2018b ; Duranti et al ., 2019 ; Modesto et al ., 2019a ; Duranti et al ., 2020 ; Modesto et al ., 2020a ; Neuzil‐Bunesova et al ., 2021 ).…”

“…In the last 3 years, a large number of novel species of the genus Bifidobacterium have been described, resulting in a genus that currently constitutes 94 different (sub)species (Duranti et al ., 2017 ; Lugli et al ., 2018b ; Modesto et al ., 2018a ; Modesto et al ., 2018c ; Modesto et al ., 2018b ; Duranti et al ., 2019 ; Modesto et al ., 2019b ; Modesto et al ., 2019a ; Duranti et al ., 2020 ; Modesto et al ., 2020b ; Modesto et al ., 2020a ; Neuzil‐Bunesova et al ., 2020 ; Neuzil‐Bunesova et al ., 2021 ). The majority of these most recently discovered novel bifidobacterial species have been isolated from mammals, in particular from faecal samples of primates, such as species of the genus Callimico , Callithrix , Saguinus and Saimiri (Duranti et al ., 2017 ; Lugli et al ., 2018b ; Modesto et al ., 2018a ; Modesto et al ., 2018c ; Modesto et al ., 2018b ; Duranti et al ., 2019 ; Modesto et al ., 2019a ; Duranti et al ., 2020 ; Modesto et al ., 2020a ; Neuzil‐Bunesova et al ., 2021 ). Nonetheless, a number of studies suggest that novel bifidobacterial species resident in the gut of Mammalia are yet to be discovered, thereby representing part of the microbial dark matter of the mammalian gut (Milani et al ., 2017a ; Alessandri et al ., 2020 ; Lugli et al ., 2020b ).…”

Bifidobacterium mizhiense sp. nov., isolated from the gut of honeybee (Apis mellifera)

“… Bifidobacterium bifidum is the type species. Based on the phylogenomic tree, ten phylogenetic groups, including the Bifidobacterium adolescentis , Bifidobacterium asteroides , Bifidobacterium bifidum , Bifidobacterium bombi , Bifidobacterium boum , Bifidobacterium longum , Bifidobacterium pseudolongum , Bifidobacterium pullorum , Bifidobacterium psychraerophilum and Bifidobacterium tissieri groups, can be recognized [2–4]. In addition to the ten phylogenetic groups, several species are still not grouped, indicating that the genus should contain more phylogenetic groups.…”