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Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily.

ABSTRACT: BACKGROUND: The extended light-harvesting complex (LHC) protein superfamily is a centerpiece of eukaryotic photosynthesis, comprising the LHC family and several families involved in photoprotection, like the LHC-like and the photosystem II subunit S (PSBS). The evolution of this complex superfamily has long remained elusive, partially due to previously missing families. RESULTS: In this study we present a meticulous search for LHC-like sequences in public genome and expressed sequence tag databases covering twelve representative photosynthetic eukaryotes from the three primary lineages of plants (Plantae): glaucophytes, red algae and green plants (Viridiplantae). By introducing a coherent classification of the different protein families based on both, hidden Markov model analyses and structural predictions, numerous new LHC-like sequences were identified and several new families were described, including the red lineage chlorophyll a/b-binding-like protein (RedCAP) family from red algae and diatoms. The test of alternative topologies of sequences of the highly conserved chlorophyll-binding core structure of LHC and PSBS proteins significantly supports the independent origins of LHC and PSBS families via two unrelated internal gene duplication events. This result was confirmed by the application of cluster likelihood mapping. CONCLUSIONS: The independent evolution of LHC and PSBS families is supported by strong phylogenetic evidence. In addition, a possible origin of LHC and PSBS families from different homologous members of the stress-enhanced protein subfamily, a diverse and anciently paralogous group of two-helix proteins, seems likely. The new hypothesis for the evolution of the extended LHC protein superfamily proposed here is in agreement with the character evolution analysis that incorporates the distribution of families and subfamilies across taxonomic lineages. Intriguingly, stress-enhanced proteins, which are universally found in the genomes of green plants, red algae, glaucophytes and in diatoms with complex plastids, could represent an important and previously missing link in the evolution of the extended LHC protein superfamily.

SUBMITTER: Engelken J

PROVIDER: S-EPMC3020630 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily.

Engelken Johannes J Brinkmann Henner H Adamska Iwona I

BMC evolutionary biology 20100730

<h4>Background</h4>The extended light-harvesting complex (LHC) protein superfamily is a centerpiece of eukaryotic photosynthesis, comprising the LHC family and several families involved in photoprotection, like the LHC-like and the photosystem II subunit S (PSBS). The evolution of this complex superfamily has long remained elusive, partially due to previously missing families.<h4>Results</h4>In this study we present a meticulous search for LHC-like sequences in public genome and expressed sequen ...[more]

PMID: 20673336

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Project description:The purple nonsulfur bacterium Rhodopseudomonas palustris is a model for understanding how a phototrophic organism adapts to changes in light intensity because it produces different light-harvesting (LH) complexes under high light (LH2) and low light intensities (LH3 and LH4). Outside of this change in the composition of the photosystem, little is understood about how R. palustris senses and responds to low light intensity. On the basis of the results of transcription analysis of 17 R. palustris strains grown in low light, we found that R. palustris strains downregulate many genes involved in iron transport and homeostasis. The only operon upregulated in the majority of R. palustris exposed to low light intensity was pucBAd, which encodes LH4. In previous work, pucBAd expression was shown to be modulated in response to light quality by bacteriophytochromes that are part of a low-light signal transduction system. Here we found that this signal transduction system also includes a redox-sensitive protein, LhfE, and that its redox sensitivity is required for LH4 synthesis in response to low light. Our results suggest that R. palustris upregulates its LH4 system when the cellular redox state is relatively oxidized. Consistent with this, we found that LH4 synthesis was upregulated under high light intensity when R. palustris was grown semiaerobically or under nitrogen-fixing conditions. Thus, changes in the LH4 system in R. palustris are not dependent on light intensity per se but rather on cellular redox changes that occur as a consequence of changes in light intensity.IMPORTANCE An essential aspect of the physiology of phototrophic bacteria is their ability to adjust the amount and composition of their light-harvesting apparatus in response to changing environmental conditions. The phototrophic purple bacterium R. palustris adapts its photosystem to a range of light intensities by altering the amount and composition of its peripheral LH complexes. Here we found that R. palustris regulates its LH4 complex in response to the cellular redox state rather than in response to light intensity per se Relatively oxidizing conditions, including low light, semiaerobic growth, and growth under nitrogen-fixing conditions, all stimulated a signal transduction system to activate LH4 expression. By understanding how LH composition is regulated in R. palustris, we will gain insight into how and why a photosynthetic organism senses and adapts its photosystem to multiple environmental cues.

Dataset Information

Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily.

Publications

Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily.

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