Genome evolution following an ecological shift in nectar-dwelling Acinetobacter

ABSTRACT The bacterial genus Acinetobacter includes species found in environmental habitats like soil and water, as well as taxa adapted to be host-associated or pathogenic. High genetic diversity may allow for this habitat flexibility, but the specific genes underlying switches between habitats are...

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Main Authors: Vivianna A. Sanchez, Tanya Renner, Lydia J. Baker, Tory A. Hendry
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:mSphere
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Online Access:https://journals.asm.org/doi/10.1128/msphere.01010-24
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author Vivianna A. Sanchez
Tanya Renner
Lydia J. Baker
Tory A. Hendry
author_facet Vivianna A. Sanchez
Tanya Renner
Lydia J. Baker
Tory A. Hendry
author_sort Vivianna A. Sanchez
collection DOAJ
description ABSTRACT The bacterial genus Acinetobacter includes species found in environmental habitats like soil and water, as well as taxa adapted to be host-associated or pathogenic. High genetic diversity may allow for this habitat flexibility, but the specific genes underlying switches between habitats are poorly understood. One lineage of Acinetobacter has undergone a substantial habitat change by evolving from a presumed soil-dwelling ancestral state to thrive in floral nectar. Here, we compared the genomes of floral-dwelling and pollinator-associated Acinetobacter, including newly described species, with genomes from relatives found in other environments to determine the genomic changes associated with this ecological shift. Following one evolutionary origin of floral nectar adaptation, nectar-dwelling Acinetobacter taxa have undergone reduction in genome size compared with relatives and have experienced dynamic gene gains and losses as they diversified. Gene content changes suggest a shift to metabolism of monosaccharides rather than diverse carbohydrates, and scavenging of nitrogen sources, which we predict to be beneficial in nectar environments. Gene gains appear to result from duplication events, evolutionary divergence, and horizontal gene transfer. Most notably, nectar-dwelling Acinetobacter acquired the ability to degrade pectin from plant pathogens, and the genes underlying this ability have duplicated and are under selection within the clade. We hypothesize that this ability was a key trait for adaptation to floral nectar, as it could improve access to nutrients in the nutritionally unbalanced habitat of nectar. These results identify the genomic changes and traits coinciding with a dramatic habitat switch from soil to floral nectar.IMPORTANCEMany bacteria, including the genus Acinetobacter, commonly evolve to exploit new habitats. However, the genetic changes that underlie habitat switches are often unknown. Floral nectar is home to specialized microbes that can grow in this nutritionally unbalanced habitat. Several specialized Acinetobacter species evolved from soil-dwelling relatives to become common and abundant in floral nectar. Here, we investigate the genomic adaptations required to successfully colonize a novel habitat like floral nectar. We performed comparative genomics analyses between nectar-dwelling Acinetobacter and Acinetobacter species from other environments, like soil and water. We find that although gene loss coincided with the switch to living in nectar, gains of specific genes from other bacteria may have been particularly important for this ecological change. Acinetobacter living in nectar gained genes for degrading pectin, a plant polysaccharide, which may improve access to nutrients in their environment. These findings shed light on how evolutionary novelty evolves in bacteria.
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spelling doaj-art-f70f12b4e4ba43eda4b7840e5ee6d3cf2025-01-28T14:00:56ZengAmerican Society for MicrobiologymSphere2379-50422025-01-0110110.1128/msphere.01010-24Genome evolution following an ecological shift in nectar-dwelling AcinetobacterVivianna A. Sanchez0Tanya Renner1Lydia J. Baker2Tory A. Hendry3Department of Microbiology, Cornell University, Ithaca, New York, USADepartment of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USADepartment of Microbiology, Cornell University, Ithaca, New York, USADepartment of Microbiology, Cornell University, Ithaca, New York, USAABSTRACT The bacterial genus Acinetobacter includes species found in environmental habitats like soil and water, as well as taxa adapted to be host-associated or pathogenic. High genetic diversity may allow for this habitat flexibility, but the specific genes underlying switches between habitats are poorly understood. One lineage of Acinetobacter has undergone a substantial habitat change by evolving from a presumed soil-dwelling ancestral state to thrive in floral nectar. Here, we compared the genomes of floral-dwelling and pollinator-associated Acinetobacter, including newly described species, with genomes from relatives found in other environments to determine the genomic changes associated with this ecological shift. Following one evolutionary origin of floral nectar adaptation, nectar-dwelling Acinetobacter taxa have undergone reduction in genome size compared with relatives and have experienced dynamic gene gains and losses as they diversified. Gene content changes suggest a shift to metabolism of monosaccharides rather than diverse carbohydrates, and scavenging of nitrogen sources, which we predict to be beneficial in nectar environments. Gene gains appear to result from duplication events, evolutionary divergence, and horizontal gene transfer. Most notably, nectar-dwelling Acinetobacter acquired the ability to degrade pectin from plant pathogens, and the genes underlying this ability have duplicated and are under selection within the clade. We hypothesize that this ability was a key trait for adaptation to floral nectar, as it could improve access to nutrients in the nutritionally unbalanced habitat of nectar. These results identify the genomic changes and traits coinciding with a dramatic habitat switch from soil to floral nectar.IMPORTANCEMany bacteria, including the genus Acinetobacter, commonly evolve to exploit new habitats. However, the genetic changes that underlie habitat switches are often unknown. Floral nectar is home to specialized microbes that can grow in this nutritionally unbalanced habitat. Several specialized Acinetobacter species evolved from soil-dwelling relatives to become common and abundant in floral nectar. Here, we investigate the genomic adaptations required to successfully colonize a novel habitat like floral nectar. We performed comparative genomics analyses between nectar-dwelling Acinetobacter and Acinetobacter species from other environments, like soil and water. We find that although gene loss coincided with the switch to living in nectar, gains of specific genes from other bacteria may have been particularly important for this ecological change. Acinetobacter living in nectar gained genes for degrading pectin, a plant polysaccharide, which may improve access to nutrients in their environment. These findings shed light on how evolutionary novelty evolves in bacteria.https://journals.asm.org/doi/10.1128/msphere.01010-24Acinetobacterplant–microbe interactionsevolutiongenomicsmicrobial ecology
spellingShingle Vivianna A. Sanchez
Tanya Renner
Lydia J. Baker
Tory A. Hendry
Genome evolution following an ecological shift in nectar-dwelling Acinetobacter
mSphere
Acinetobacter
plant–microbe interactions
evolution
genomics
microbial ecology
title Genome evolution following an ecological shift in nectar-dwelling Acinetobacter
title_full Genome evolution following an ecological shift in nectar-dwelling Acinetobacter
title_fullStr Genome evolution following an ecological shift in nectar-dwelling Acinetobacter
title_full_unstemmed Genome evolution following an ecological shift in nectar-dwelling Acinetobacter
title_short Genome evolution following an ecological shift in nectar-dwelling Acinetobacter
title_sort genome evolution following an ecological shift in nectar dwelling acinetobacter
topic Acinetobacter
plant–microbe interactions
evolution
genomics
microbial ecology
url https://journals.asm.org/doi/10.1128/msphere.01010-24
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AT lydiajbaker genomeevolutionfollowinganecologicalshiftinnectardwellingacinetobacter
AT toryahendry genomeevolutionfollowinganecologicalshiftinnectardwellingacinetobacter