TY - JOUR

T1 - Phylogenomic analysis and metabolic role reconstruction of mutualistic Rhizobiales hindgut symbionts of Acromyrmex leaf-cutting ants

AU - Zhukova, Mariya

AU - Sapountzis, Panagiotis

AU - Schiott, Morten

AU - Boomsma, Jacobus J.

PY - 2022

Y1 - 2022

N2 - Rhizobiales are well-known plant-root nitrogen-fixing symbionts, but the functions of insect-associated Rhizobiales are poorly understood. We obtained genomes of three strains associated with Acromyrmex leaf-cutting ants and show that, in spite of being extracellular gut symbionts, they lost all pathways for essential amino acid biosynthesis, making them fully dependent on their hosts. Comparison with 54 Rhizobiales genomes showed that all insect-associated Rhizobiales lost the ability to fix nitrogen and that the Acromyrmex symbionts had exceptionally also lost the urease genes. However, the Acromyrmex strains share biosynthesis pathways for riboflavin vitamin, queuosine and a wide range of antioxidant enzymes likely to be beneficial for the ant fungus-farming symbiosis. We infer that the Rhizobiales symbionts catabolize excess of fungus-garden-derived arginine to urea, supplementing complementary Mollicutes symbionts that turn arginine into ammonia and infer that these combined symbiont activities stabilize the fungus-farming mutualism. Similar to the Mollicutes symbionts, the Rhizobiales species have fully functional CRISPR/Cas and R-M phage defenses, suggesting that these symbionts are important enough for the ant hosts to have precluded the evolution of metabolically cheaper defenseless strains.Analysis of genomes of Rhizobiales symbionts of Acromyrmex reveals a dependence of these bacteria on their host, while they supply ants with compounds that enhance the robustness of the mutualism.

AB - Rhizobiales are well-known plant-root nitrogen-fixing symbionts, but the functions of insect-associated Rhizobiales are poorly understood. We obtained genomes of three strains associated with Acromyrmex leaf-cutting ants and show that, in spite of being extracellular gut symbionts, they lost all pathways for essential amino acid biosynthesis, making them fully dependent on their hosts. Comparison with 54 Rhizobiales genomes showed that all insect-associated Rhizobiales lost the ability to fix nitrogen and that the Acromyrmex symbionts had exceptionally also lost the urease genes. However, the Acromyrmex strains share biosynthesis pathways for riboflavin vitamin, queuosine and a wide range of antioxidant enzymes likely to be beneficial for the ant fungus-farming symbiosis. We infer that the Rhizobiales symbionts catabolize excess of fungus-garden-derived arginine to urea, supplementing complementary Mollicutes symbionts that turn arginine into ammonia and infer that these combined symbiont activities stabilize the fungus-farming mutualism. Similar to the Mollicutes symbionts, the Rhizobiales species have fully functional CRISPR/Cas and R-M phage defenses, suggesting that these symbionts are important enough for the ant hosts to have precluded the evolution of metabolically cheaper defenseless strains.Analysis of genomes of Rhizobiales symbionts of Acromyrmex reveals a dependence of these bacteria on their host, while they supply ants with compounds that enhance the robustness of the mutualism.

KW - antioxidants

KW - complementary mutualistic functionality

KW - CRISPR

KW - Cas

KW - domestication

KW - gene loss

KW - riboflavin

KW - GUT MICROBIOTA

KW - BACTERIAL

KW - RIBOFLAVIN

KW - GENOME

KW - EVOLUTION

KW - ENZYMES

KW - CLASSIFICATION

KW - RESTRICTION

KW - DIVERSITY

KW - ALIGNMENT

U2 - 10.1093/femsec/fiac084

DO - 10.1093/femsec/fiac084

M3 - Journal article

C2 - 35906195

VL - 98

JO - F E M S Microbiology Reviews

JF - F E M S Microbiology Reviews

SN - 0168-6445

IS - 9

M1 - fiac084

ER -