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Bridging the divide: bacteria synthesizing archaeal membrane lipids

Laura Villanueva, F. A. Bastiaan von Meijenfeldt, Alexander B. Westbye, Ellen C. Hopmans, Bas E. Dutilh, Jaap S. Sinninghe Damste

Preprint posted on 19 October 2018 https://www.biorxiv.org/content/early/2018/10/19/448035

and

Extensive transfer of membrane lipid biosynthetic genes between Archaea and Bacteria

Gareth A. Coleman, Richard D. Pancost, Tom A. Williams

Preprint posted on 2 May 2018 https://www.biorxiv.org/content/early/2018/05/02/312991

Straddling the lipid divide: evidence that archaea and bacteria have exchanged lipid biosynthesis genes in the past, and that a present-day Black Sea bacterium might possess a mixed membrane

Selected by Dey Lab

[Note added 2018/10/26: Coleman et al. released an updated version of their preprint on the 25th of October, which includes additional analyses and updated figures. The broad conclusions of the manuscript remain unchanged. You can find the updated preprint here. Figure 1 is taken from the updated preprint (Coleman et al. 2018b).

 

Context

The genomes of bacteria and archaea, the two primary domains of life, provide strong support for a conserved core of universal genes and the idea that there was once a single primordial cellular lineage- the Last Universal Common Ancestor (LUCA)1. Yet, extant archaea and bacteria differ in striking ways, including a critical difference in membrane chemistry2 (Figure 1).  The isoprenoid ether-linked glycerol-1-phosphate (G1P) lipids of archaea and the acyl ester-linked G3P lipids of bacteria, at first glance, could not appear more different- from the unique enzyme cascades needed to produce them down to the chirality of the backbone.

 

Figure 1, reproduced in full from Coleman et al. 2018b under a Creative Commons CC-BY 4.0 international license. a) The canonical ether/ester biosynthetic pathways in Archaea and Bacteria and how they relate to glycerol metabolism. Based on Figure 1 from Villanueva et al (2016). Archaeal pathways in blue and yellow (blue=heterotrophic Archaea, yellow=autotrophic Archaea), bacterial pathway in red. Hypothetical biosynthetic pathway, as suggested by Villanueva et al. (2016), in dashed lines. b) Composition of bacterial and archaeal phospholipids. In Archaea, G1P is synthesised from dihydroxyacetone phosphate (DHAP) using the enzymes glycerol-1-phosphate dehydrogenase (G1PDH). The first and second isoprenoid chains (GGGPs) are added by geranylgeranylglyceryl synthase (GGGPS) and digeranylgeranylglyceryl synthase (DGGGPS) respectively. In Bacteria, G3P is synthesised by glycerol-3-phosphate dehydrogenase (G3PDH) from DHAP. There are two forms of this enzyme, encoded by the gpsA and glp genes respectively. G3P may also be produced from glycerol by glycerol kinase (glpK). In certain Bacteria, such as Gammaproteobacteria, the first fatty-acid chain is added by a version of glycerol-3-phosphate acyltransferase encoded by the PlsB gene. Other Bacteria, including most gram positive bacteria, use a system which includes another glycerol-3-phosphate acyltransferase encoded by PlsY, in conjunction with an enzyme encoded by PlsX (Yao and Rock 2013; Parsons and Rock 2013). The second fattyacid chain is attached by 1-acylglycerol-3-phosphate O-acyltransferase, encode by PlsC.

 

The consequences of this apparent “lipid divide”3 for theories of cellular evolution are momentous. For example, did LUCA even have a membrane, or was it an acellular entity occupying a porous substrate4? Did early eukaryotes, whose extant representatives possess bacterial-type lipid chemistry, eliminate the membrane lipids of their likely archaeal ancestor, and did they necessarily transition through a heterochiral intermediate5?

 As it turns out, though, a growing body of experimental and genomic evidence suggests that the lipid divide might be narrower than once thought, setting the stage for the two preprints highlighted here. Notably, Bacillus subtilis has been shown to make both bacterial and archaeal lipids6; earlier this year, an engineered E. coli strain equipped with a mix of the right bacterial and archaeal enzymes was shown to stably maintain a mixed heterochiral membrane7.

Major findings 

Coleman et al. investigate the distribution and phylogeny of the core phospholipid biosynthesis enzymes outlined in Figure 1 across bacteria and archaea. They find that the archaeal enzymes are widely prevalent in bacterial lineages. With all 3 core archaeal enzymes present, some species of the Firmicutes, Actinobacteria and Fibrobacteres lineages probably make G1P phospholipids. The story is a bit less clear for species belonging to the other two-thirds of the FBC group (Fibrobacteres, Bacteroidetes and Chlorobi) which have GGGPS and DGGGPS orthologs but no G1PDH.  Examining transfers in the other direction, the bacterial enzymes appeared more sporadically in the archaeal genomes, with no phylum containing homologs of all the genes and more than half containing none.

Coleman et al. go on to construct rooted Bayesian single-gene phylogenies for their set of core biosynthetic genes. Using these phylogenies, they suggest that G1PDH was either present in LUCA or transferred very early from stem archaea to bacterial groups or the bacterial stem; GGGPS probably duplicated once pre-LUCA, with evidence of two distinct paralogs; DGGGPS was either present in LUCA or transferred to bacteria multiple times from the archaea. In contrast, the roots for the bacterial enzyme trees lie (albeit weakly) within the bacterial domain, with concomitant evidence of multiple recent transfers to archaea. Thus, a tentative yet striking conclusion from the study is that the archaeal synthesis pathway might be older than the bacterial one.

It is worth noting, as the authors do point out, that transfer timing-related conclusions must necessarily be treated with caution given the uncertainty in placing the roots for trees spanning such large evolutionary distances. For those interested, I strongly recommend a deep dive into the extensive discussion of rooting strategies detailed in the manuscript.

Villanueva et al. describe the discovery and metagenomic assembly of 4 novel, near-complete Candidatus Cloacimonetes genomes (belonging to the FBC/FCB group) sampled from the deep waters of the Black Sea. First, they find genes consistent with the biosynthesis of canonical bacterial membranes, including G3P synthesis and esterification. They also identify bona-fide GGGPS and DGGGP synthase homologs, proximally located in the genome and with high homology to their archaeal counterparts. Importantly, they also identify matching gene transcripts in the Black Sea samples.

When expressed in E. coli, a recombinant Ca. Cloacimonetes GGGPS catalyzes the formation of GGGP from GGPP. Co-expressing GGGPS and DGGGP in E. coli (engineered to produce the right precursors) leads to the production of phosphatidylglycerol archaeol, consistent with the hypothesis that these enzymes could be producing bona fide archaeal-type lipids in vivo.

Echoing the findings of Coleman et al., Villanueva et al. point out that their metagenomic assemblies are missing the first enzyme in the cascade- G1PDH (Figure 1)- as well as its bacterial homolog. This is not necessarily a problem, as E. coli engineered to make heterochiral membranes can produce G1P lipids without either enzyme7, suggesting that bacteria possess an alternative G1P synthesis pathway. It remains a formal possibility, however, that the Ca. Cloacimonetes genes are actually making G3P lipids, or are involved in a catabolic rather than anabolic pathway.

 

Outlook

The studies highlighted here add to the growing consensus that archaea and bacteria have the capacity to mix and match their phospholipid biosynthesis pathways, much like many other facets of their metabolism and cell biology.

What does this mean for models of cellular evolution? Models analysing the LUCA can no longer rely on the existence of a strict lipid divide as proof that the first cells had no membrane, and must now contend with the possibility that the archaeal lipid biosynthesis pathway might be significantly older than the bacterial one.

The challenge for models of eukaryogenesis is twofold. First, the next generation of models must include the possibility that the archaeal host and/or bacterial endosymbiont already possessed mixed or heterochiral membranes. There is some evidence that genomes of the Asgard clade of archaea, closest known archaeal relatives to eukaryotes, encode components of both bacterial-type and archaeal-type lipid biosynthesis pathways8. Second, if mixed membranes are stable, the ensuing loss of heterochirality in the proto-eukaryote will require an additional explanation (based on environmental factors, for example).

 

References:

  1. Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).
  2. Lombard, J., López-García, P. & Moreira, D. The early evolution of lipid membranes and the three domains of life. Nat. Rev. Microbiol. 10, 507–515 (2012).
  3. Koga, Y. Early Evolution of Membrane Lipids: How did the Lipid Divide Occur? J. Mol. Evol. 72, 274–282 (2011).
  4. Martin, W. & Russell, M. J. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. B Biol. Sci. 358, 59–85 (2003).
  5. Baum, D. A. A comparison of autogenous theories for the origin of eukaryotic cells. Am. J. Bot. 102, 1954–65 (2015).
  6. Guldan, H., Matysik, F.-M., Bocola, M., Sterner, R. & Babinger, P. Functional Assignment of an Enzyme that Catalyzes the Synthesis of an Archaea-Type Ether Lipid in Bacteria. Angew. Chemie Int. Ed. 50, 8188–8191 (2011).
  7. Caforio, A. et al. Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. Proc. Natl. Acad. Sci. U. S. A. 115, 3704–3709 (2018).
  8. Villanueva, L., Schouten, S. & Damsté, J. S. S. Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the ‘lipid divide’. Environ. Microbiol. 19, 54–69 (2017).

 

Tags: cellular evolution, heterochiral membranes, leca, lipid divide, luca

Posted on: 21 October 2018 , updated on: 26 October 2018

doi: https://doi.org/10.1242/prelights.5230

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Authors' comment

Gareth Coleman and Tom Williams shared about Extensive transfer of membrane lipid biosynthetic genes between Archaea and Bacteria

Thanks for the interest in our work. One thing that seems quite clear now is that there’s a growing body of evidence (our trees, but also a number of important previous studies using outgroup rooting) that some of the genes involved in making membranes are shared between Bacteria and Archaea. It hasn’t been clear what these shared genes might be doing when they are found in the “other” domain, which is why the new work by Villanueva et al. is so interesting: it shows that in Cloacimonetes, the archaeal genes can support the production of archaeal-type membrane phospholipids, at least when heterologously expressed in E. coli.

One finding from our work that could be of general interest is that outgroup-free rooting can be a viable (perhaps complementary) approach to traditional outgroup rooting, especially when the branch leading to the outgroup is long. There are certainly lots of other interesting questions in early evolution where being able to root gene trees would be useful.

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