Anoxygenic phototroph pufLM gene sequences derived from tropical aquatic sampling sites: Diversity, distribution, and phylogenetics

Purple sulfur bacteria (PSB) and purple non-sulfur bacteria (PNSB) are characterized by their ability to perform anoxygenic photosynthesis. PSB and PNSB are ubiquitously found in coastal waters, enclosed lagoons, stagnant water, mangrove soils, estuaries, and similar environments. In this study, we examine microbial diversity in PSB enrichments derived from a variety of tropical sampling sites (e.g., Thailand, Puerto Rico) associated with shrimp ponds, coastal mangroves, fresh water ponds, and Nymphaeaceae (i.e., water lily) plant tissue. Since 16S rRNA-based analyses are inadequate to describe the diversity of phototrophic bacteria, other biomarkers (e.g., pufLM) are used to construct phylogenies and elucidate biogeography. Our samples indicate that the majority of sequences associated with freshwater pond PSB were related to known marine, halophilic, or salt-tolerant PSB (e.g., Marichromatium, Allochromatium, Thiococcus, and Thiohalocapsa). Phylotypes not closely-associated with known species of PSB (or PNSB) were also found. PNSB gene sequences, which appear to be related to Rhodopseudomonas and Rhodoplanes, were mostly found in freshwater samples and from Nymphaeaceae plant tissues, suggesting a difference in the ecology and distribution of these two broader bacterial groups. This difference is likely due to differences in habitat such as physical (e.g., temperature) and chemical parameters (e.g., salinity). Our preliminary analyses demonstrate a rich diversity of anoxygenic phototrophic bacteria from tropical sampling sites. Few studies have described the diversity of purple bacteria in tropical environments using full pufLM gene sequences. Employing next-generation sequencing (NGS) appears to provide greater resolution towards a deeper understanding of the global diversity and distribution of these anoxygenic phototrophs.

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Competition between anoxygenic phototrophic bacteria and colorless sulfur bacteria in a microbial mat

FEMS Microbiology Ecology ◽

10.1016/0168-6496(92)90071-z ◽

1992 ◽

Vol 101 (1) ◽

pp. 51-58 ◽

Cited By ~ 4

Author(s):

P Visscher

Keyword(s):

Phototrophic Bacteria ◽

Microbial Mat ◽

Anoxygenic Phototrophic Bacteria ◽

Sulfur Bacteria ◽

Colorless Sulfur Bacteria

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Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria

Archives of Microbiology ◽

10.1007/s00203-004-0718-9 ◽

2004 ◽

Vol 182 (4) ◽

pp. 265-276 ◽

Cited By ~ 85

Author(s):

Niels-Ulrik Frigaard ◽

Donald A. Bryant

Keyword(s):

Photosynthetic Apparatus ◽

Green Sulfur Bacteria ◽

Phototrophic Bacteria ◽

Anoxygenic Phototrophic Bacteria ◽

Green Bacteria ◽

Sulfur Bacteria ◽

Green Sulfur

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Distribution and Origin of Oxygen-Dependent and Oxygen-Independent Forms of Mg-Protoporphyrin Monomethylester Cyclase among Phototrophic Proteobacteria

Applied and Environmental Microbiology ◽

10.1128/aem.00104-13 ◽

2013 ◽

Vol 79 (8) ◽

pp. 2596-2604 ◽

Cited By ~ 26

Author(s):

Ekaterina N. Boldareva-Nuianzina ◽

Zuzana Bláhová ◽

Roman Sobotka ◽

Michal Koblížek

Keyword(s):

Protoporphyrin Ix ◽

Phototrophic Bacteria ◽

Purple Sulfur Bacteria ◽

Content Type ◽

Anoxygenic Phototrophs ◽

Genome Data ◽

Sulfur Bacteria ◽

Independent Form ◽

Dependent Form ◽

Photosynthesis Gene

ABSTRACTMagnesium-protoporphyrin IX monomethylester cyclase is one of the key enzymes of the bacteriochlorophyll biosynthesis pathway. There exist two fundamentally different forms of this enzyme. The oxygen-dependent form, encoded by the geneacsF, catalyzes the formation of the bacteriochlorophyll fifth ring using oxygen, whereas the oxygen-independent form encoded by the genebchEutilizes an oxygen atom extracted from water. The presence ofacsFandbchEgenes was surveyed in various phototrophicProteobacteriausing the available genomic data and newly designed degenerated primers. It was found that while the majority of purple nonsulfur bacteria contained both forms of the cyclase, the purple sulfur bacteria contained only the oxygen-independent form. All tested species of aerobic anoxygenic phototrophs containedacsFgenes, but some of them also retained thebchEgene. In contrast tobchEphylogeny, theacsFphylogeny was in good agreement with 16S inferred phylogeny. Moreover, the survey of the genome data documented that theacsFgene occupies a conserved position inside the photosynthesis gene cluster, whereas thebchElocation in the genome varied largely between the species. This suggests that the oxygen-dependent cyclase was recruited by purple phototrophic bacteria very early during their evolution. The primary sequence and immunochemical similarity with its cyanobacterial counterparts suggests thatacsFmay have been acquired byProteobacteriavia horizontal gene transfer from cyanobacteria. The acquisition of the gene allowed purple nonsulfur phototrophic bacteria to proliferate in the mildly oxygenated conditions of the Proterozoic era.

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Competition between anoxygenic phototrophic bacteria and colorless sulfur bacteria in a microbial mat

FEMS Microbiology Letters ◽

10.1111/j.1574-6968.1992.tb05761.x ◽

1992 ◽

Vol 101 (1) ◽

pp. 51-58 ◽

Cited By ~ 2

Author(s):

Pieter T. Visscher ◽

Frank P. Ende ◽

Bartholomeus E.M. Schaub ◽

Hans Gemerden

Keyword(s):

Phototrophic Bacteria ◽

Microbial Mat ◽

Anoxygenic Phototrophic Bacteria ◽

Sulfur Bacteria ◽

Colorless Sulfur Bacteria

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Phylogeny of Anoxygenic Photosynthesis Based on Sequences of Photosynthetic Reaction Center Proteins and a Key Enzyme in Bacteriochlorophyll Biosynthesis, the Chlorophyllide Reductase

Microorganisms ◽

10.3390/microorganisms7110576 ◽

2019 ◽

Vol 7 (11) ◽

pp. 576 ◽

Cited By ~ 7

Author(s):

Johannes F. Imhoff ◽

Tanja Rahn ◽

Sven Künzel ◽

Sven C. Neulinger

Keyword(s):

16S Rrna ◽

Reaction Center ◽

Purple Bacteria ◽

Photosynthetic Reaction Center ◽

Phototrophic Bacteria ◽

Anoxygenic Phototrophic Bacteria ◽

Type Ii ◽

Phylogenetic Relations ◽

Key Enzyme ◽

Bacteriochlorophyll Biosynthesis

Photosynthesis is a key process for the establishment and maintenance of life on earth, and it is manifested in several major lineages of the prokaryote tree of life. The evolution of photosynthesis in anoxygenic photosynthetic bacteria is of major interest as these have the most ancient roots of photosynthetic systems. The phylogenetic relations between anoxygenic phototrophic bacteria were compared on the basis of sequences of key proteins of the type-II photosynthetic reaction center, including PufLM and PufH (PuhA), and a key enzyme of bacteriochlorophyll biosynthesis, the light-independent chlorophyllide reductase BchXYZ. The latter was common to all anoxygenic phototrophic bacteria, including those with a type-I and those with a type-II photosynthetic reaction center. The phylogenetic considerations included cultured phototrophic bacteria from several phyla, including Proteobacteria (138 species), Chloroflexi (five species), Chlorobi (six species), as well as Heliobacterium modesticaldum (Firmicutes), Chloracidobacterium acidophilum (Acidobacteria), and Gemmatimonas phototrophica (Gemmatimonadetes). Whenever available, type strains were studied. Phylogenetic relationships based on a photosynthesis tree (PS tree, including sequences of PufHLM-BchXYZ) were compared with those of 16S rRNA gene sequences (RNS tree). Despite some significant differences, large parts were congruent between the 16S rRNA phylogeny and photosynthesis proteins. The phylogenetic relations demonstrated that bacteriochlorophyll biosynthesis had evolved in ancestors of phototrophic green bacteria much earlier as compared to phototrophic purple bacteria and that multiple events independently formed different lineages of aerobic phototrophic purple bacteria, many of which have very ancient roots. The Rhodobacterales clearly represented the youngest group, which was separated from other Proteobacteria by a large evolutionary gap.

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Competition between anoxygenic phototrophic bacteria and colorless sulfur bacteria in a microbial mat

FEMS Microbiology Ecology ◽

10.1111/j.1574-6941.1992.tb01648.x ◽

1992 ◽

Vol 10 (1) ◽

pp. 51-58 ◽

Cited By ~ 36

Author(s):

Pieter T. Visscher ◽

Frank P. Ende ◽

Bartholomeus E. M. Schaub ◽

Hans Gemerden

Keyword(s):

Phototrophic Bacteria ◽

Microbial Mat ◽

Anoxygenic Phototrophic Bacteria ◽

Sulfur Bacteria ◽

Colorless Sulfur Bacteria

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Distribution and characterization of phototrophic bacteria isolated from the water of Bietri Bay (Ebrie Lagoon, Ivory Coast)

Canadian Journal of Microbiology ◽

10.1139/m84-042 ◽

1984 ◽

Vol 30 (3) ◽

pp. 273-284 ◽

Cited By ~ 15

Author(s):

Pierre Caumette

Keyword(s):

Ivory Coast ◽

Lower Layer ◽

Purple Bacteria ◽

Rhodopseudomonas Palustris ◽

Phototrophic Bacteria ◽

Sulfur Bacteria ◽

Oxygenated Water ◽

Chlorobium Phaeobacteroides ◽

Microaerobic Conditions ◽

Synthetic Media

Phototrophic bacteria were observed forming a brown layer, at the interface between aerobic and anaerobic waters, in a stratified tropical lagoon (Bietri Bay, 5°15′ N, 4 °W, Ivory Coast). Within the brown layer (3.2–4 m depth), a stratification of different genera was observed. In the upper part purple bacteria developed, whereas green and brown Chlorobiaceae abounded mostly in a lower layer (3.5–4 m depth). Among the purple bacteria, some species were isolated and identified as Rhodopseudomonas palustris, Chromatium violascens, Chr. vinosum, and Chr. gracile. The green and brown sulfur bacteria were related to Chlorobium vibrioforme and Chl. phaeobacteroides. Chlorobium phaeobacteroides was the most abundant organism in the whole brown layer as well as in the deepest layer. As the phototrophic bacteria isolated were able to grow at different salt concentrations, the stratification observed could be explained by the gradients of sulfide and light. As shown by experimental data, purple bacteria grew under microaerobic conditions and used light intensities higher than green and brown sulfur bacteria whose growths were highly dependent on strict anaerobic conditions. During the dry season, holomixis involved the disappearance of the brown layer. Some phototrophic bacteria were found in the oxygenated water column. However, only brown Chlorobium was isolated. Although this species was found in a microaerobic environment in Bietri Bay, it never grew under microaerobic conditions in the synthetic media. This bacterium (Chlorobium phaeobacteroides strain BI 28) was able to use thiosulfate, as did Chl. vibrioforme isolated from the brown layer.

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Structural and Spectroscopic Properties of a Reaction Center Complex from the Chlorosome-Lacking Filamentous Anoxygenic Phototrophic Bacterium Roseiflexus castenholzii

Journal of Bacteriology ◽

10.1128/jb.187.5.1702-1709.2005 ◽

2005 ◽

Vol 187 (5) ◽

pp. 1702-1709 ◽

Cited By ~ 30

Author(s):

Mitsunori Yamada ◽

Hui Zhang ◽

Satoshi Hanada ◽

Kenji V. P. Nagashima ◽

Keizo Shimada ◽

...

Keyword(s):

Reaction Center ◽

Phylogenetic Trees ◽

Light Harvesting ◽

Purple Bacteria ◽

Photosynthetic Apparatus ◽

Spectroscopic Properties ◽

Phototrophic Bacteria ◽

Amino Acid Sequences ◽

Anoxygenic Phototrophic Bacteria ◽

Reading Frame

ABSTRACT The photochemical reaction center (RC) complex of Roseiflexus castenholzii, which belongs to the filamentous anoxygenic phototrophic bacteria (green filamentous bacteria) but lacks chlorosomes, was isolated and characterized. The genes coding for the subunits of the RC and the light-harvesting proteins were also cloned and sequenced. The RC complex was composed of L, M, and cytochrome subunits. The cytochrome subunit showed a molecular mass of approximately 35 kDa, contained hemes c, and functioned as the electron donor to the photo-oxidized special pair of bacteriochlorophylls in the RC. The RC complex appeared to contain three molecules of bacteriochlorophyll and three molecules of bacteriopheophytin, as in the RC preparation from Chloroflexus aurantiacus. Phylogenetic trees based on the deduced amino acid sequences of the RC subunits suggested that R. castenholzii had diverged from C. aurantiacus very early after the divergence of filamentous anoxygenic phototrophic bacteria from purple bacteria. Although R. castenholzii is phylogenetically related to C. aurantiacus, the arrangement of its puf genes, which code for the light-harvesting proteins and the RC subunits, was different from that in C. aurantiacus and similar to that in purple bacteria. The genes are found in the order pufB, -A, -L, -M, and -C, with the pufL and pufM genes forming one continuous open reading frame. Since the photosynthetic apparatus and genes of R. castenholzii have intermediate characteristics between those of purple bacteria and C. aurantiacus, it is likely that they retain many features of the common ancestor of purple bacteria and filamentous anoxygenic phototrophic bacteria.

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