TY - JOUR
T1 - A possible aquatic origin of the Thiaminase TenA of the human gut symbiont Bacteroides thetaiotaomicron
AU - Stentz, Régis
AU - Cheema, Jitender
AU - Philo, Mark
AU - Carding, Simon R.
N1 - Funding Information: This research was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) Institute Strategic Programme Grant Gut Microbes and Health BB/R012490/1 and its constituent project(s) BBS/E/F/000PR10353 (Theme 1, Determinants of microbe-host responses in the gut across life), and the BBSRC Core Capability Grant BB/CCG1860/1.
PY - 2023/8
Y1 - 2023/8
N2 - TenA thiamin-degrading enzymes are commonly found in prokaryotes, plants, fungi and algae and are involved in the thiamin salvage pathway. The gut symbiont Bacteroides thetaiotaomicron (Bt) produces a TenA protein (BtTenA) which is packaged into its extracellular vesicles. An alignment of BtTenA protein sequence with proteins from different databases using the basic local alignment search tool (BLAST) and the generation of a phylogenetic tree revealed that BtTenA is related to TenA-like proteins not only found in a small number of intestinal bacterial species but also in some aquatic bacteria, aquatic invertebrates, and freshwater fish. This is, to our knowledge, the first report describing the presence of TenA-encoding genes in the genome of members of the animal kingdom. By searching metagenomic databases of diverse host-associated microbial communities, we found that BtTenA homologues were mostly represented in biofilms present on the surface of macroalgae found in Australian coral reefs. We also confirmed the ability of a recombinant BtTenA to degrade thiamin. Our study shows that BttenA-like genes which encode a novel sub-class of TenA proteins are sparingly distributed across two kingdoms of life, a feature of accessory genes known for their ability to spread between species through horizontal gene transfer.
AB - TenA thiamin-degrading enzymes are commonly found in prokaryotes, plants, fungi and algae and are involved in the thiamin salvage pathway. The gut symbiont Bacteroides thetaiotaomicron (Bt) produces a TenA protein (BtTenA) which is packaged into its extracellular vesicles. An alignment of BtTenA protein sequence with proteins from different databases using the basic local alignment search tool (BLAST) and the generation of a phylogenetic tree revealed that BtTenA is related to TenA-like proteins not only found in a small number of intestinal bacterial species but also in some aquatic bacteria, aquatic invertebrates, and freshwater fish. This is, to our knowledge, the first report describing the presence of TenA-encoding genes in the genome of members of the animal kingdom. By searching metagenomic databases of diverse host-associated microbial communities, we found that BtTenA homologues were mostly represented in biofilms present on the surface of macroalgae found in Australian coral reefs. We also confirmed the ability of a recombinant BtTenA to degrade thiamin. Our study shows that BttenA-like genes which encode a novel sub-class of TenA proteins are sparingly distributed across two kingdoms of life, a feature of accessory genes known for their ability to spread between species through horizontal gene transfer.
KW - Bacterial extracellular vesicles
KW - Horizontal gene transfer
KW - Monophyletic group
KW - Thiamin
UR - http://www.scopus.com/inward/record.url?scp=85151957164&partnerID=8YFLogxK
U2 - 10.1007/s00239-023-10101-8
DO - 10.1007/s00239-023-10101-8
M3 - Article
C2 - 37022443
AN - SCOPUS:85151957164
SN - 0022-2844
VL - 91
SP - 482
EP - 491
JO - Journal of Molecular Evolution
JF - Journal of Molecular Evolution
IS - 4
ER -