Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes
The human intestinal microbiota that comprise over 1,000 species thrive in dark and anaerobic environments. They are recognized for the production of diverse low-molecular-weight metabolites crucial to human health and diseases. Carotenoids, low-molecular-weight pigments known for their antioxidativ...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-06-01
|
| Series: | Engineering Microbiology |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2667370324000109 |
| _version_ | 1797234282193747968 |
|---|---|
| author | Wataru Matsumoto Miho Takemura Haruka Nanaura Yuta Ami Takashi Maoka Kazutoshi Shindo Shin Kurihara Norihiko Misawa |
| author_facet | Wataru Matsumoto Miho Takemura Haruka Nanaura Yuta Ami Takashi Maoka Kazutoshi Shindo Shin Kurihara Norihiko Misawa |
| author_sort | Wataru Matsumoto |
| collection | DOAJ |
| description | The human intestinal microbiota that comprise over 1,000 species thrive in dark and anaerobic environments. They are recognized for the production of diverse low-molecular-weight metabolites crucial to human health and diseases. Carotenoids, low-molecular-weight pigments known for their antioxidative activity, are delivered to humans through oral intake. However, it remains unclear whether human intestinal bacteria biosynthesize carotenoids as part of the in-situ microbiota. In this study, we investigated carotenoid synthesis genes in various human gut and probiotic bacteria. As a result, novel candidates, the crtM and crtN genes, were identified in the carbon monoxide-utilizing gut anaerobe Eubacterium limosum and the lactic acid bacterium Leuconostoc mesenteroides subsp. mesenteroides. These gene candidates were isolated, introduced into Escherichia coli, which synthesized a carotenoid substrate, and cultured aerobically. Structural analysis of the resulting carotenoids revealed that the crtM and crtN gene candidates of E. limosum and L. mesenteroides mediate the production of 4,4′-diaponeurosporene through 15-cis-4,4′-diapophytoene. Evaluation of the crtE-homologous genes in these bacteria indicated their non-functionality for C40-carotenoid production. E. limosum and L. mesenteroides, along with the known carotenogenic lactic acid bacterium Lactiplantibacillus plantarum, were observed to produce no carotenoids under strictly anaerobic conditions. The two lactic acid bacteria synthesized detectable levels of 4,4′-diaponeurosporene under semi-aerobic conditions. The findings highlight that the obligate anaerobe E. limosum retains aerobically functional C30-carotenoid biosynthesis genes, potentially with no immediate self-utility, suggesting an evolutionary direction in carotenoid biosynthesis. (229 words) |
| first_indexed | 2024-04-24T16:29:35Z |
| format | Article |
| id | doaj.art-a724f99982bd465c8ae5079ebab75a84 |
| institution | Directory Open Access Journal |
| issn | 2667-3703 |
| language | English |
| last_indexed | 2024-04-24T16:29:35Z |
| publishDate | 2024-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Engineering Microbiology |
| spelling | doaj.art-a724f99982bd465c8ae5079ebab75a842024-03-30T04:40:21ZengElsevierEngineering Microbiology2667-37032024-06-0142100147Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genesWataru Matsumoto0Miho Takemura1Haruka Nanaura2Yuta Ami3Takashi Maoka4Kazutoshi Shindo5Shin Kurihara6Norihiko Misawa7Research Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, 1-308, Suematsu, Nonoich-shi 921-8836, JapanResearch Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, 1-308, Suematsu, Nonoich-shi 921-8836, Japan; Corresponding authors.Research Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, 1-308, Suematsu, Nonoich-shi 921-8836, JapanDepartment of Science and Technology on Food Safety, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, JapanResearch Institute for Production Development, Shimogamo-morimotocho, Sakyo-ku, Kyoto 606-0805, JapanDepartment of Food and Nutrition, Japan Women's University, Mejirodai, Bunkyo-ku, Tokyo 112-8681, JapanDepartment of Science and Technology on Food Safety, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, JapanResearch Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, 1-308, Suematsu, Nonoich-shi 921-8836, Japan; Corresponding authors.The human intestinal microbiota that comprise over 1,000 species thrive in dark and anaerobic environments. They are recognized for the production of diverse low-molecular-weight metabolites crucial to human health and diseases. Carotenoids, low-molecular-weight pigments known for their antioxidative activity, are delivered to humans through oral intake. However, it remains unclear whether human intestinal bacteria biosynthesize carotenoids as part of the in-situ microbiota. In this study, we investigated carotenoid synthesis genes in various human gut and probiotic bacteria. As a result, novel candidates, the crtM and crtN genes, were identified in the carbon monoxide-utilizing gut anaerobe Eubacterium limosum and the lactic acid bacterium Leuconostoc mesenteroides subsp. mesenteroides. These gene candidates were isolated, introduced into Escherichia coli, which synthesized a carotenoid substrate, and cultured aerobically. Structural analysis of the resulting carotenoids revealed that the crtM and crtN gene candidates of E. limosum and L. mesenteroides mediate the production of 4,4′-diaponeurosporene through 15-cis-4,4′-diapophytoene. Evaluation of the crtE-homologous genes in these bacteria indicated their non-functionality for C40-carotenoid production. E. limosum and L. mesenteroides, along with the known carotenogenic lactic acid bacterium Lactiplantibacillus plantarum, were observed to produce no carotenoids under strictly anaerobic conditions. The two lactic acid bacteria synthesized detectable levels of 4,4′-diaponeurosporene under semi-aerobic conditions. The findings highlight that the obligate anaerobe E. limosum retains aerobically functional C30-carotenoid biosynthesis genes, potentially with no immediate self-utility, suggesting an evolutionary direction in carotenoid biosynthesis. (229 words)http://www.sciencedirect.com/science/article/pii/S2667370324000109C30 carotenoid biosynthesisObligate anaerobeHuman gut bacteriumEubacterium limosumLeuconostoc mesenteroidesLactiplantibacillus plantarum |
| spellingShingle | Wataru Matsumoto Miho Takemura Haruka Nanaura Yuta Ami Takashi Maoka Kazutoshi Shindo Shin Kurihara Norihiko Misawa Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes Engineering Microbiology C30 carotenoid biosynthesis Obligate anaerobe Human gut bacterium Eubacterium limosum Leuconostoc mesenteroides Lactiplantibacillus plantarum |
| title | Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes |
| title_full | Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes |
| title_fullStr | Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes |
| title_full_unstemmed | Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes |
| title_short | Carotenoid productivity in human intestinal bacteria Eubacterium limosum and Leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes |
| title_sort | carotenoid productivity in human intestinal bacteria eubacterium limosum and leuconostoc mesenteroides with functional analysis of their carotenoid biosynthesis genes |
| topic | C30 carotenoid biosynthesis Obligate anaerobe Human gut bacterium Eubacterium limosum Leuconostoc mesenteroides Lactiplantibacillus plantarum |
| url | http://www.sciencedirect.com/science/article/pii/S2667370324000109 |
| work_keys_str_mv | AT watarumatsumoto carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT mihotakemura carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT harukananaura carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT yutaami carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT takashimaoka carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT kazutoshishindo carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT shinkurihara carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes AT norihikomisawa carotenoidproductivityinhumanintestinalbacteriaeubacteriumlimosumandleuconostocmesenteroideswithfunctionalanalysisoftheircarotenoidbiosynthesisgenes |