Temperature change elicits lipidome adaptation in Mycoplasma mycoides and JCVI-syn3B

Safronova, N.; Junghans, L.; Sáenz, J. P. (2024) Cell Reports, 43(7), 114435. DOI: 10.1016/j.celrep.2024.114435

Summary

We used shotgun lipidomics to characterize temperature-dependent lipidome adaptation in [[mycoplasma-mycoides|Mycoplasma mycoides]] and the minimal cell JCVI-Syn3B. Despite their reduced genomes, both organisms exhibit lipidome flexibility in response to temperature change. Lipid abundances follow a universal logarithmic distribution shared across eukaryotes and bacteria, with comparable degrees of remodeling regardless of organismal complexity. Temporal analysis revealed a two-stage cold adaptation process: a swift shift in cholesterol and cardiolipin levels followed by gradual acyl chain modifications. Critically, JCVI-Syn3B showed impaired head-group-specific acyl chain remodeling compared to M. mycoides, associated with impaired homeoviscous adaptation.

Key Findings

• Lipid abundances in M. mycoides and JCVI-Syn3B follow a universal logarithmic rank-abundance distribution, a pattern shared from minimal cells to yeast to mammals.
• Both organisms exhibit lipidome flexibility despite genomic simplification, but the extent of remodeling differs between M. mycoides (more flexible) and Syn3B (more constrained).
• Head-group-specific acyl chain remodeling — identified as a hallmark of lipidome adaptation in [[methylobacterium-extorquens|Methylobacterium extorquens]] (Chwastek et al., 2020, Cell Reports) — is deficient in Syn3B, correlating with impaired homeoviscous adaptation.
• Two-stage temporal cold adaptation: (1) rapid changes in cholesterol and cardiolipin abundance within hours, followed by (2) slower acyl chain saturation adjustments over days.
• This work establishes M. mycoides and Syn3B as minimal membrane model systems for studying lipidome design principles.

Methods

• Shotgun lipidomics: quantitative mass spectrometry of M. mycoides and JCVI-Syn3B lipidomes across temperatures (25–42 °C).
• Temporal sampling: lipidomes measured at multiple time points after temperature shift to capture fast and slow adaptation phases.
• Membrane viscosity: DCVJ-based plate reader method (Chwastek et al., 2019, ChemBioChem) to assess homeoviscous adaptation.

Significance

This paper demonstrated that even organisms with near-minimal genomes retain the capacity for lipidome adaptation, but that genome reduction compromises the sophistication of that adaptation. The universal lipid rank-abundance distribution suggests deep constraints on lipidome organization across all domains of life.