Gains and losses of metabolic function inferred from a phylotranscriptomic analysis of algae

Abstract

Hidden Markov models representing 167 protein sequence families were used to infer the presence or absence of homologs within the transcriptomes of 183 algal species/strains. Statistical analyses of the distribution of HMM hits across major clades of algae, or at branch points on the phylogenetic tree of 98 chlorophytes, confirmed and extended known cases of metabolic loss and gain, most notably the loss of the mevalonate pathway for terpenoid synthesis in green algae but not, as we show here, in the streptophyte algae. Evidence for novel events was found as well, most remarkably in the recurrent and coordinated gain or loss of enzymes for the glyoxylate shunt. We find, as well, a curious pattern of retention (or re-gain) of HMG-CoA synthase in chlorophytes that have otherwise lost the mevalonate pathway, suggesting a novel, co-opted function for this enzyme in select lineages. Finally, we find striking, phylogenetically linked distributions of coding sequences for three pathways that synthesize the major membrane lipid phosphatidylcholine, and a complementary phylogenetic distribution pattern for the non-phospholipid DGTS (diacyl-glyceryl-trimethylhomoserine). Mass spectrometric analysis of lipids from 25 species was used to validate the inference of DGTS synthesis from sequence data.

Artificial protein sequences enable recognition of vicinal and distant protein functional relationships

“…These clan members possess the Rossmann domain that binds nicotinamide adenine dinucleotide phosphate (NADP) as a co‐factor. Hearteningly, other reports propose that this family is likely involved in diacylglyceryl‐N,N,N‐trimethylhomoserine synthesis involving gene products of BtaA and BtaB 48 . BtaA is shown to encode the DUF sequences while BtaB encodes a methyl transferase 49,50 .…”

“…Hearteningly, other reports propose that this family is likely involved in diacylglyceryl-N,N,N-trimethylhomoserine synthesis involving gene products of BtaA and BtaB. 48 BtaA is shown to encode the DUF sequences while BtaB encodes a methyl transferase. 49,50 Our association of the DUF3419 family with methyl transferase of the NADP_Rossmann clan reaffirms this association.…”

Occurrence, Evolution and Specificities of Iron-Sulfur Proteins and Maturation Factors in Chloroplasts from Algae

“…Isoprenoid synthesis relies on two pathways, the mevalonate (MVA) pathway, which does not involve Fe-S proteins, and the 2-C-methyl-d-erythritol 4-phosphate (MEP) pathway, which requires two proteins with (4Fe-4S) clusters: (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase (HDS, ISPG) and 4-hydroxy-3-methylbut-2-en-1-yl diphosphate reductase (HDR, ISPH). The MVA pathway is present in animals, fungi and archaea, the MEP pathway is present in nearly all bacteria [ 58 ]. Plants have usually retained both pathways.…”

“…Plants have usually retained both pathways. Most of the plant-specific isoprenoids, such as phytols and carotenoids, are synthesized in plastids by the MEP pathway inherited from the cyanobacterium endosymbiont [ 58 , 59 , 60 ], while the cytosolic MVA pathway contributes to sterol synthesis [ 61 ]. The situation is variable in microalgae.…”

“…The situation is variable in microalgae. In Archaeplastids, Charophytes possess both pathways but Chlorophytes and some Rhodophytes rely only on the MEP pathway for isoprenoid synthesis, although the HMG-CoA synthase, the second enzyme of the MVA pathway, is present in some of them [ 58 , 60 ]. For algae with secondary endosymbiosis, diatoms and Euglena gracilis kept both pathways [ 61 , 62 ], while only the MEP pathway is present in Nannochloropis oceanica , although a HMG-CoA synthase is also present in this alga [ 63 ].…”