Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders
Abstract Background Bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a bacterial second messenger that affects diverse processes in different bacteria, including the cell cycle, motility, and biofilm formation. Its cellular levels are controlled by the opposing activities of two type...
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-022-09072-9 |
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| author | Sonja Koppenhöfer Andrew S. Lang |
| author_facet | Sonja Koppenhöfer Andrew S. Lang |
| author_sort | Sonja Koppenhöfer |
| collection | DOAJ |
| description | Abstract Background Bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a bacterial second messenger that affects diverse processes in different bacteria, including the cell cycle, motility, and biofilm formation. Its cellular levels are controlled by the opposing activities of two types of enzymes, with synthesis by diguanylate cyclases containing a GGDEF domain and degradation by phosphodiesterases containing either an HD-GYP or an EAL domain. These enzymes are ubiquitous in bacteria with up to 50 encoded in some genomes, the specific functions of which are mostly unknown. Results We used comparative analyses to identify genomic patterns among genes encoding proteins with GGDEF, EAL, and HD-GYP domains in five orders of the class Alphaproteobacteria. GGDEF-containing sequences and GGDEF-EAL hybrids were the most abundant and had the highest diversity of co-occurring auxiliary domains while EAL and HD-GYP containing sequences were less abundant and less diverse with respect to auxiliary domains. There were striking patterns in the chromosomal localizations of the genes found in two of the orders. The Rhodobacterales’ EAL-encoding genes and Rhizobiales’ GGDEF-EAL-encoding genes showed opposing patterns of distribution compared to the GGDEF-encoding genes. In the Rhodobacterales, the GGDEF-encoding genes showed a tri-modal distribution with peaks mid-way between the origin (ori) and terminus (ter) of replication and at ter while the EAL-encoding genes peaked near ori. The patterns were more complex in the Rhizobiales, but the GGDEF-encoding genes were biased for localization near ter. Conclusions The observed patterns in the chromosomal localizations of these genes suggest a coupling of synthesis and hydrolysis of c-di-GMP with the cell cycle. Moreover, the higher proportions and diversities of auxiliary domains associated with GGDEF domains and GGDEF-EAL hybrids compared to EAL or HD-GYP domains could indicate that more stimuli affect synthesis compared to hydrolysis of c-di-GMP. |
| first_indexed | 2024-04-11T12:35:45Z |
| format | Article |
| id | doaj.art-9bdd6ab430a349c3b64abf2004e66d02 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-11T12:35:45Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-9bdd6ab430a349c3b64abf2004e66d022022-12-22T04:23:38ZengBMCBMC Genomics1471-21642022-12-0123111310.1186/s12864-022-09072-9Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial ordersSonja Koppenhöfer0Andrew S. Lang1Department of Biology, Memorial University of NewfoundlandDepartment of Biology, Memorial University of NewfoundlandAbstract Background Bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a bacterial second messenger that affects diverse processes in different bacteria, including the cell cycle, motility, and biofilm formation. Its cellular levels are controlled by the opposing activities of two types of enzymes, with synthesis by diguanylate cyclases containing a GGDEF domain and degradation by phosphodiesterases containing either an HD-GYP or an EAL domain. These enzymes are ubiquitous in bacteria with up to 50 encoded in some genomes, the specific functions of which are mostly unknown. Results We used comparative analyses to identify genomic patterns among genes encoding proteins with GGDEF, EAL, and HD-GYP domains in five orders of the class Alphaproteobacteria. GGDEF-containing sequences and GGDEF-EAL hybrids were the most abundant and had the highest diversity of co-occurring auxiliary domains while EAL and HD-GYP containing sequences were less abundant and less diverse with respect to auxiliary domains. There were striking patterns in the chromosomal localizations of the genes found in two of the orders. The Rhodobacterales’ EAL-encoding genes and Rhizobiales’ GGDEF-EAL-encoding genes showed opposing patterns of distribution compared to the GGDEF-encoding genes. In the Rhodobacterales, the GGDEF-encoding genes showed a tri-modal distribution with peaks mid-way between the origin (ori) and terminus (ter) of replication and at ter while the EAL-encoding genes peaked near ori. The patterns were more complex in the Rhizobiales, but the GGDEF-encoding genes were biased for localization near ter. Conclusions The observed patterns in the chromosomal localizations of these genes suggest a coupling of synthesis and hydrolysis of c-di-GMP with the cell cycle. Moreover, the higher proportions and diversities of auxiliary domains associated with GGDEF domains and GGDEF-EAL hybrids compared to EAL or HD-GYP domains could indicate that more stimuli affect synthesis compared to hydrolysis of c-di-GMP.https://doi.org/10.1186/s12864-022-09072-9PhosphodiesteraseDiguanylate cyclaseDNA replicationCell cycleHD-GYPGGDEF |
| spellingShingle | Sonja Koppenhöfer Andrew S. Lang Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders BMC Genomics Phosphodiesterase Diguanylate cyclase DNA replication Cell cycle HD-GYP GGDEF |
| title | Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders |
| title_full | Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders |
| title_fullStr | Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders |
| title_full_unstemmed | Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders |
| title_short | Patterns of abundance, chromosomal localization, and domain organization among c-di-GMP-metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders |
| title_sort | patterns of abundance chromosomal localization and domain organization among c di gmp metabolizing genes revealed by comparative genomics of five alphaproteobacterial orders |
| topic | Phosphodiesterase Diguanylate cyclase DNA replication Cell cycle HD-GYP GGDEF |
| url | https://doi.org/10.1186/s12864-022-09072-9 |
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