A Ca2+-binding motif underlies the unusual properties of certain photosynthetic bacterial core light-harvesting complexes

Abstract

The mildly thermophilic purple phototrophic bacterium Allochromatium tepidum provides a unique model for investigating various intermediate phenotypes observed between those of thermophilic and mesophilic counterparts. The core light-harvesting (LH1) complex from A. tepidum exhibits an absorption maximum at 890 nm and mildly enhanced thermostability, both of which are Ca2+-dependent. However, it is unknown what structural determinants might contribute to these properties. Here, we present a cryo-EM structure of the reaction center–associated LH1 complex at 2.81 Å resolution, in which we identify multiple pigment-binding α- and β-polypeptides within an LH1 ring. Of the 16 α-polypeptides, we show that six (α1) bind Ca2+ along with β1- or β3-polypeptides to form the Ca2+-binding sites. This structure differs from that of fully Ca2+-bound LH1 from Thermochromatium tepidum, enabling determination of the minimum structural requirements for Ca2+-binding. We also identified three amino acids (Trp44, Asp47, and Ile49) in the C-terminal region of the A. tepidum α1-polypeptide that ligate each Ca ion, forming a Ca2+-binding WxxDxI motif that is conserved in all Ca2+-bound LH1 α-polypeptides from other species with reported structures. The partial Ca2+-bound structure further explains the unusual phenotypic properties observed for this bacterium in terms of its Ca2+-requirements for thermostability, spectroscopy, and phototrophic growth, and supports the hypothesis that A. tepidum may represent a “transitional” species between mesophilic and thermophilic purple sulfur bacteria. The characteristic arrangement of multiple αβ-polypeptides also suggests a mechanism of molecular recognition in the expression and/or assembly of the LH1 complex that could be regulated through interactions with reaction center subunits. The mildly thermophilic purple phototrophic bacterium Allochromatium tepidum provides a unique model for investigating various intermediate phenotypes observed between those of thermophilic and mesophilic counterparts. The core light-harvesting (LH1) complex from A. tepidum exhibits an absorption maximum at 890 nm and mildly enhanced thermostability, both of which are Ca2+-dependent. However, it is unknown what structural determinants might contribute to these properties. Here, we present a cryo-EM structure of the reaction center–associated LH1 complex at 2.81 Å resolution, in which we identify multiple pigment-binding α- and β-polypeptides within an LH1 ring. Of the 16 α-polypeptides, we show that six (α1) bind Ca2+ along with β1- or β3-polypeptides to form the Ca2+-binding sites. This structure differs from that of fully Ca2+-bound LH1 from Thermochromatium tepidum, enabling determination of the minimum structural requirements for Ca2+-binding. We also identified three amino acids (Trp44, Asp47, and Ile49) in the C-terminal region of the A. tepidum α1-polypeptide that ligate each Ca ion, forming a Ca2+-binding WxxDxI motif that is conserved in all Ca2+-bound LH1 α-polypeptides from other species with reported structures. The partial Ca2+-bound structure further explains the unusual phenotypic properties observed for this bacterium in terms of its Ca2+-requirements for thermostability, spectroscopy, and phototrophic growth, and supports the hypothesis that A. tepidum may represent a “transitional” species between mesophilic and thermophilic purple sulfur bacteria. The characteristic arrangement of multiple αβ-polypeptides also suggests a mechanism of molecular recognition in the expression and/or assembly of the LH1 complex that could be regulated through interactions with reaction center subunits. Bacterial photosynthetic antennae have evolved diverse strategies to optimize their spectral and thermodynamic properties for adaptation to changing environments. For the core light-harvesting complex (LH1) of purple phototrophic bacteria, the first thoroughly investigated case was that of the thermophilic sulfur bacterium, Thermochromatium tepidum, a phototroph isolated from a hot spring microbial mat in Yellowstone National Park (USA) and capable of growth up to 57 °C (1Madigan M.T. A novel photosynthetic bacterium isolated from a Yellowstone hot spring.Science. 1984; 225: 313-315Crossref PubMed Scopus (98) Google Scholar). This bacterium incorporates calcium ions into its LH1 complex, resulting in an enhanced thermostability and a red-shifted absorption maximum (Qy transition) at 915 nm (2Kimura Y. Hirano Y. Yu L.-J. Suzuki H. Kobayashi M. Wang Z.-Y. Calcium ions are involved in the unusual red shift of the light-harvesting 1 Qy transition of the core complex in thermophilic purple sulfur bacterium Thermochromatium tepidum.J. Biol. Chem. 2008; 283: 13867-13873Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar, 3Kimura Y. Yu L.-J. Hirano Y. Suzuki H. Wang Z.-Y. Calcium ions are required for the enhanced thermal stability of the light-harvesting-reaction center core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum.J. Biol. Chem. 2009; 284: 93-99Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar, 4Ma F. Kimura Y. Yu L.-J. Wang P. Ai X.-C. Wang Z.-Y. Zhang J.-P. Specific Ca2+-binding motif in the LH1 complex from photosynthetic bacterium Thermochromatium tepidum as revealed by optical spectroscopy and structural modeling.FEBS J. 2009; 276: 1739-1749Crossref PubMed Scopus (26) Google Scholar, 5Kimura Y. Inada Y. Numata T. Arikawa T. Li Y. Zhang J.-P. Wang Z.-Y. Ohno T. Metal cations modulate the bacteriochlorophyll-protein interaction in the light-harvesting 1 core complex from Thermochromatium tepidum.Biochim. Biophys. Acta – Bioenerg. 2012; 1817: 1022-1029Crossref Scopus (26) Google Scholar, 6Li Y. Kimura Y. Arikawa T. Wang-Otomo Z.-Y. Ohno T. ATR-FTIR detection of metal-sensitive structural changes in the light-harvesting 1 reaction center complex from the thermophilic purple sulfur bacterium Thermochromatium tepidum.Biochemistry. 2013; 52: 9001-9008Crossref PubMed Scopus (13) Google Scholar). Subsequent crystallographic structure of the T. tepidum LH1 in a reaction center (RC)-associated form identified 16 Ca2+-binding sites in the LH1 complex (7Niwa S. Yu L.-J. Takeda K. Hirano Y. Kawakami T. Wang-Otomo Z.-Y. Miki K. Structure of the LH1-RC complex from Thermochromatium tepidum at 3.0 Å.Nature. 2014; 508: 228-232Crossref PubMed Scopus (160) Google Scholar), each Ca2+ being bound by a pair of αβ-polypeptides and two water molecules (8Yu L.-J. Suga M. Wang-Otomo Z.-Y. Shen J.-R. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution.Nature. 2018; 556: 209-213Crossref PubMed Scopus (69) Google Scholar). This Ca2+-binding network tightly locks the LH1 ring and contributes to both its thermostability and Qy redshift (9Ma F. Yu L.-J. Wang-Otomo Z.-Y. van Grondelle R. The origin of the unusual Qy red shift in LH1-RC complexes from purple bacteria Thermochromatium tepidum as revealed by Stark absorption spectroscopy.Biochim. Biophys. Acta – Bioenerg. 2015; 1847: 1479-1486Crossref Scopus (25) Google Scholar, 10Kimura Y. Yura Y. Hayashi Y. Li Y. Onoda M. Yu L.-J. Wang-Otomo Z.-Y. Ohno T. Spectroscopic and thermodynamic characterization of the metal-binding sites in the LH1-RC complex from thermophilic photosynthetic bacterium Thermochromatium tepidum.J. Phys. Chem. B. 2016; 120: 12466-12473Crossref PubMed Scopus (11) Google Scholar, 11Ma F. Yu L.-J. Hendrikx R. Wang-Otomo Z.-Y. van Grondelle R. Direct observation of energy detrapping in LH1-RC complex by two-dimensional electronic spectroscopy.J. Am. Chem. Soc. 2017; 139: 591-594Crossref PubMed Scopus (16) Google Scholar). The dual role of Ca2+ in affecting LH1 properties was also demonstrated in a second case where the mesophilic purple sulfur bacterium Thiorhodovibrio (Trv.) strain 970 was shown to integrate Ca2+ into its LH1 complex (12Permentier H.P. Neerken S. Overmann J. Amesz J. A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm.Biochemistry. 2001; 40: 5573-5578Crossref PubMed Scopus (42) Google Scholar, 13Imanishi M. Takenouchi M. Takaichi S. Nakagawa S. Saga Y. Takenaka S. M.T. Overmann J. Wang-Otomo Z.-Y. Kimura Y. A dual role for Ca2+ in the spectral and stability of light-harvesting 1 reaction center of purple phototrophic PubMed Scopus Google Scholar), an redshift of its LH1 to the red-shifted Qy of all bacteriochlorophyll A cryo-EM structure of the strain 970 complex revealed that 16 Ca2+ are present in the LH1 C-terminal and a network the structural of the unique LH1 redshift K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google Scholar). a mechanism contributes to the thermostability of the LH1 of a thermophilic purple bacterium M.T. Takaichi S. Wang-Otomo Z.-Y. A. K. H. Y. a thermophilic species of the bacteriochlorophyll PubMed Scopus Google Scholar, R. Takaichi S. T. R. M. Takenaka S. Y. M.T. Wang-Otomo Z.-Y. Kimura Y. thermostability from a thermophilic PubMed Scopus Google Scholar). This with to its mesophilic However, thermostability, the B. absorption R. Takaichi S. T. R. M. Takenaka S. Y. M.T. Wang-Otomo Z.-Y. Kimura Y. thermostability from a thermophilic PubMed Scopus Google Scholar). also intermediate for the LH1 complexes that various properties in between those of thermophilic and mesophilic purple sulfur bacteria. is the isolated from a mildly thermophilic purple sulfur bacterium Allochromatium tepidum M.T. M. Takaichi S. Y. H. Wang-Otomo Z.-Y. tepidum, a hot spring species of purple sulfur PubMed Scopus Google Scholar). This a between the of the thermophilic T. tepidum and mesophilic Allochromatium The complex from A. tepidum an absorption at 890 nm and a mildly enhanced thermostability Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar). of the properties are and intermediate between those of T. tepidum and A. Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar), Ca ions A. tepidum that in the T. tepidum This observation to the A. tepidum in and we present its cryo-EM The structure identified six Ca ions in the LH1 complex that are bound to a motif in α-polypeptides and into and thermodynamic of the A. tepidum the of the A. tepidum complex the structural arrangement of multiple of αβ-polypeptides in the LH1 ring that the intermediate properties of this complex with those of T. tepidum and A. The cryo-EM structure of A. tepidum was at 2.81 Å and and and its structure with T. tepidum (8Yu L.-J. Suga M. Wang-Otomo Z.-Y. Shen J.-R. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution.Nature. 2018; 556: 209-213Crossref PubMed Scopus (69) Google and strain 970 K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google Scholar). The A. tepidum LH1 a ring structure of 16 of and 16 that are the 1 and the LH1 α- and β-polypeptides in the of and two of identified in the which are with and Ca ions in the that are bound to the LH1 and β-polypeptides and and The Ca2+ is with that by spectroscopy Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar). The a and two a at the and a at the The the of the LH1 with the and in to the LH1 in the region of the in the are unique the LH1 α-polypeptides, and an role in assembly of the motif and arrangement of the Allochromatium tepidum LH1 multiple of the from the of the of the arrangement of the LH1 in the as in the of the and sites. The Ca2+-bound αβ-polypeptides are to the with The are shown in red in the of and β3-polypeptides are shown in The region a of the and to the that the Ca2+-binding motif is present in the of the A. tepidum α1-polypeptide with those of A. T. tepidum and strain 970 to the The Ca2+-binding motif of T. tepidum and strain 970 is present in the A. in the A. tepidum and A. is by an light-harvesting reaction to we to all three of the α-polypeptides in the A. tepidum LH1 from the cryo-EM six and A and bind Ca ions their of and and of as and This WxxDxI Ca2+-binding motif is present in the A. tepidum LH1 and However, that the motif is conserved in all Ca2+-bound LH1 α-polypeptides of T. tepidum (8Yu L.-J. Suga M. Wang-Otomo Z.-Y. Shen J.-R. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution.Nature. 2018; 556: 209-213Crossref PubMed Scopus (69) Google and strain 970 K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google The in this motif is the in the A. LH1 α1-polypeptide is a and the LH1 bind Ca2+ Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar). that the amino is for Ca2+-binding the is a The Ca2+-binding sites by A. tepidum LH1 and are to the LH1 a The of and also form with the of a of the α1-polypeptide with and revealed that the of the the the a from that of the α1-polypeptide the a both and are to bind this of its LH1 a is of the are and to have for the a with Ca2+-binding those that bind Ca2+ The is to with the Qy energy J. and bacteriochlorophyll optical of with structural Phys. Chem. Scopus Google Scholar, K. The crystallographic structure of the light-harvesting complex from the purple bacteria strain 2001; 40: PubMed Scopus Google Scholar). are between the Ca2+-bound and in terms of the between the of the and the of the for the and a of the and with those from other bacteria are in of the LH1 in the A. tepidum are to those of the A. LH1 M.T. M. Takaichi S. Y. H. Wang-Otomo Z.-Y. tepidum, a hot spring species of purple sulfur PubMed Scopus Google Scholar). and are the A. tepidum was in the LH1 complex is that the was also in the A. LH1 Z.-Y. M. Suzuki H. Kobayashi M. T. and characterization of the of core light-harvesting complexes from purple sulfur PubMed Scopus Google Scholar). The of A. tepidum form with β3-polypeptides pair with a mechanism of molecular recognition between the The are through and interactions in the and the interaction in the The is at a to the of the LH1 ring of the purple bacterium K. R. S. R. M. Yu L.-J. Kimura Y. M.T. A. Wang-Otomo Z.-Y. A in the LH1-RC PubMed Scopus Google and a with the to its with the and into two and the two of the LH1 The arrangement is by interactions between the LH1 and the and in the region A. tepidum LH1 and have interactions with the in the these have and are to with the through their C-terminal The C-terminal of the is with the and C-terminal of the of the also with the the The of the is of the LH1 ring where the and two of the and in are with the characteristic of the LH1 the to the that the unique arrangement of the A. tepidum LH1 α-polypeptides is by interactions with the subunits. of amino between the A. tepidum Ca2+-bound α1-polypeptide and T. tepidum revealed an in the C-terminal region of the A. tepidum α1-polypeptide A is also present at the in the A. LH1 this is to both the within the and the Ca2+-binding the the was to the LH1 absorption maximum (Qy transition) (2Kimura Y. Hirano Y. Yu L.-J. Suzuki H. Kobayashi M. Wang Z.-Y. Calcium ions are involved in the unusual red shift of the light-harvesting 1 Qy transition of the core complex in thermophilic purple sulfur bacterium Thermochromatium tepidum.J. Biol. Chem. 2008; 283: 13867-13873Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar, 13Imanishi M. Takenouchi M. Takaichi S. Nakagawa S. Saga Y. Takenaka S. M.T. Overmann J. Wang-Otomo Z.-Y. Kimura Y. A dual role for Ca2+ in the spectral and stability of light-harvesting 1 reaction center of purple phototrophic PubMed Scopus Google Scholar, M. K. Takaichi S. S. Yu L.-J. Y. K. Kawakami T. Takenouchi T. Y. A. Ohno T. Shen J.-R. K. in in a S. A. 2017; PubMed Scopus Google Scholar). Here, structure of the A. tepidum LH1 that the in the α1-polypeptide is in a region the The of the was by forming a was to a affecting both and Ca2+-binding sites an A. tepidum and A. or T. in this region have a the transition in of these However, the in the between A. tepidum and T. tepidum suggests that the LH1 complex of the thermophilic T. tepidum may have evolved to a in this region in to thermal and the T. tepidum LH1 to at that growth of A. The multiple LH1 complex of A. tepidum a unique model to the minimum structural for Ca2+-binding in photosynthetic LH1 This was with the fully Ca2+-bound reported from T. tepidum (8Yu L.-J. Suga M. Wang-Otomo Z.-Y. Shen J.-R. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution.Nature. 2018; 556: 209-213Crossref PubMed Scopus (69) Google and strain 970 K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google all LH1 in the complexes of these bacteria in Ca2+-binding and have amino the Ca2+-binding it to the of However, the LH1 complexes from T. tepidum and strain the A. tepidum LH1 complex both Ca2+-bound and in a for an of the for Ca2+-binding. Of the 16 A. tepidum LH1 α-polypeptides, six of the α1-polypeptide bind Ca2+ to form Ca2+-binding sites with β1- or amino acids (Trp44, Asp47, and Ile49) in the C-terminal region of A. tepidum α1-polypeptide identified as the that form a Ca2+-binding WxxDxI This structural motif the minimum for an LH1 to be to bind Ca2+ and is conserved in all Ca2+-bound α-polypeptides with reported structures. is that the WxxDxI motif is also present in the LH1 α-polypeptides of and A. B. K. Overmann J. and of light-harvesting complexes of three absorption 2012; PubMed Scopus (11) Google Scholar). the LH1 complexes from these purple sulfur bacteria bind Ca2+ is the of this motif is The Ca2+-bound structure of the A. tepidum LH1 explains its intermediate properties in terms of thermostability, spectroscopy, and phototrophic growth Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google with the fully Ca2+-bound LH1 of the thermophilic T. tepidum and the LH1 of the mesophilic A. The A. tepidum is that of A. Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar). The A. tepidum an transition at 890 nm to that of A. from that of T. tepidum The Ca2+-requirements for an thermostability, and phototrophic growth of A. tepidum also those of T. tepidum Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar). of the interactions these intermediate properties is the between and LH1 that is by Ca2+-binding. The between the and the in the of LH1 by spectroscopy revealed with the Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google Scholar). the fully Ca2+-bound T. tepidum LH1 the and exhibits the Qy redshift by the Ca2+-bound A. tepidum in the is from that of T. tepidum is that of the A. be by The between the and the are Å and Å for the A. tepidum α- and are the Å and Å for the T. tepidum α- and β-polypeptides that the in A. tepidum LH1 are those in T. The with a partial Ca2+-binding in A. tepidum LH1 contribute to its thermostability that of T. tepidum structural with and that these properties are with the Ca2+ of the LH1 and is with that Ca ions tightly the LH1 by forming a network that contributes to both thermostability and the redshift (8Yu L.-J. Suga M. Wang-Otomo Z.-Y. Shen J.-R. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution.Nature. 2018; 556: 209-213Crossref PubMed Scopus (69) Google Scholar, K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google Scholar). also the hypothesis that A. tepidum is a in the of the phenotypic between mesophilic and thermophilic purple sulfur bacteria. from structural of this is by and of A. tepidum M.T. M. Takaichi S. Y. H. Wang-Otomo Z.-Y. tepidum, a hot spring species of purple sulfur PubMed Scopus Google Scholar). of the molecules the have investigated J. and bacteriochlorophyll optical of with structural Phys. Chem. Scopus Google Scholar, J. B. amino acids as determinants for in S. A. PubMed Google Scholar, J. of in Am. Chem. Soc. Scopus Google Scholar, T. of energy structure to 2009; PubMed Scopus Google Scholar). is a between the of the Qy and the and of the ring of or ring in at these J. of in Am. Chem. Soc. Scopus Google Scholar, A. P. in of Phys. Chem. B. Scopus Google Scholar, F. J. A. B. H. T. energy in the S. A. PubMed Scopus Google Scholar, L.-J. Kawakami T. Kimura Y. Wang-Otomo Z.-Y. for the unusual Qy and enhanced thermostability of the LH1 complex from Thermochromatium tepidum.Biochemistry. 2016; PubMed Scopus Google Scholar). The Ca ions in A. tepidum and T. tepidum LH1 are at with a of Å from the of a and as from the revealed that these Ca ions the interaction network and in the LH1 Qy transition L.-J. Kawakami T. Kimura Y. Wang-Otomo Z.-Y. for the unusual Qy and enhanced thermostability of the LH1 complex from Thermochromatium tepidum.Biochemistry. 2016; PubMed Scopus Google Scholar). the other energy from the LH1 a to the also investigated the T. tepidum LH1 and its F. Kimura Y. Wang P. Wang Z.-Y. Zhang J.-P. of two spectral of the core complexes from photosynthetic bacterium Thermochromatium J. 2008; Full Text Full Text PDF PubMed Scopus Google Scholar, F. Yu L.-J. Wang-Otomo Z.-Y. van Grondelle R. energy in purple bacteria tepidum with A to thermal energy in Biophys. 2016; PubMed Scopus Google Scholar, Y. K. S. Takenouchi M. Suzuki K. R. M. Takenaka S. M.T. Wang-Otomo Z.-Y. and of a light-harvesting reaction center core 2018; PubMed Scopus Google Scholar). an the energy shown to be to those for other phototrophic bacteria that show at that of energy from the LH1 to is by these The arrangement of multiple within the A. tepidum LH1 ring is also differs from that of multiple LH1 complex from strain 970 K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google in of of the and of the α-polypeptides the The A. tepidum pair with β3-polypeptides to form and the pair with and are and in the A. tepidum LH1 multiple of both and in strain 970 form with β1- or K. R. Y. M. Takenouchi M. M. Yu L.-J. Overmann J. M.T. Kimura Y. A. Wang-Otomo Z.-Y. structure of a Ca2+-bound photosynthetic LH1-RC complex multiple PubMed Scopus Google Scholar). The multiple and in A. tepidum LH1 form two and are the of the core with the in to the and in the all in strain 970 are of the and all are the with the of and in to the in the region the A. tepidum a of the Ca2+-bound into two may also the of Ca2+-binding thermostability and both properties are all in the LH1 ring. The characteristic arrangement of the A. tepidum LH1 αβ-polypeptides is regulated in its expression and/or assembly through multiple interactions within the LH1 complex α- and β-polypeptides through and/or and between LH1 and the with the and in the and C-terminal of the with the cryo-EM structure of the A. tepidum LH1 complex, an amino of in the C-terminal region of the Ca2+-bound α1-polypeptide to have the and Ca2+-binding sites the this that the of this in T. tepidum α-polypeptides may be a for its redshift at 915 nm a mechanism to the other of an at the in the T. tepidum α-polypeptides in a strain LH1 an absorption maximum at nm M. K. Takaichi S. S. Yu L.-J. Y. K. Kawakami T. Takenouchi T. Y. A. Ohno T. Shen J.-R. K. in in a S. A. 2017; PubMed Scopus Google Scholar). could be by of two or both the T. tepidum α-polypeptides may a in the region from that of the A. tepidum LH1 structural changes at the and/or Ca2+-binding and the in the T. tepidum LH1 may have a from that of in the A. tepidum LH1 α1-polypeptide as in the Ca2+-binding motif where the was shown to an role for Ca2+-binding this structural be required the A. LH1 complex of A. tepidum at °C for of the A. tepidum the Y. S. A. K. A. Ohno T. Takaichi S. M.T. Wang-Otomo Z.-Y. of calcium ions the thermostability and properties of the LH1-RC complex from a thermophilic purple bacterium Allochromatium tepidum.J. Phys. Chem. B. 2017; PubMed Scopus Google with The was a with and at by a of from to and with for the by a and of the LH1 by and F. K. Y. Y. Yu L.-J. Kobayashi M. 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