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Link to original content: https://pubmed.ncbi.nlm.nih.gov/14566056/
Proteorhodopsin genes are distributed among divergent marine bacterial taxa - PubMed Skip to main page content
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. 2003 Oct 28;100(22):12830-5.
doi: 10.1073/pnas.2133554100. Epub 2003 Oct 17.

Proteorhodopsin genes are distributed among divergent marine bacterial taxa

José R de la Torre  1 , Lynne M Christianson, Oded Béjà, Marcelino T Suzuki, David M Karl, John Heidelberg, Edward F DeLong
Affiliations

Proteorhodopsin genes are distributed among divergent marine bacterial taxa

José R de la Torre et al. Proc Natl Acad Sci U S A. .

Abstract

Proteorhodopsin (PR) is a retinal-binding bacterial integral membrane protein that functions as a light-driven proton pump. The gene encoding this photoprotein was originally discovered on a large genome fragment derived from an uncultured marine gamma-proteobacterium of the SAR86 group. Subsequently, many variants of the PR gene have been detected in marine plankton, via PCR-based gene surveys. It has not been clear, however, whether these different PR genes are widely distributed among different bacterial groups, or whether they have a restricted taxonomic distribution. We report here comparative analyses of PR-bearing genomic fragments recovered directly from planktonic bacteria inhabiting the California coast, the central Pacific Ocean, and waters offshore the Antarctica Peninsula. Sequence analysis of an Antarctic genome fragment harboring PR (ANT32C12) revealed moderate conservation in gene order and identity, compared with a previously reported PR-containing genome fragment from a Monterey Bay gamma-proteobacterium (EBAC31A08). Outside the limited region of synteny shared between these clones, however, no significant DNA or protein identity was evident. Analysis of a third PR-containing genome fragment (HOT2C01) from the North Pacific subtropical gyre showed even more divergence from the gamma-proteobacterial PR-flanking region. Subsequent phylogenetic and comparative genomic analyses revealed that the Central North Pacific PR-containing genome fragment (HOT2C01) originated from a planktonic alpha-proteobacterium. These data indicate that PR genes are distributed among a variety of divergent marine bacterial taxa, including both alpha- and gamma-proteobacteria. Our analyses also demonstrate the utility of cultivation-independent comparative genomic approaches for assessing gene content and distribution in naturally occurring microbes.

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Figures

Fig. 1.
Fig. 1.
Gene content and organization of PR gene-containing genomic fragments recovered from environmental samples. The alignment of the genome fragments is based on the position of the PR gene. Regions of similarity in gene content and organization between different genome fragments are connected by shaded areas. BCF, Bacteroides-Cytophagales-Flavobacterium group; Gram +, Gram-positive bacteria. Each colored bar represents one ORF. The color of each bar depicts the phylogenetic origin of the highest ranking blast match to each predicted ORF (see Tables 1–5). Small insertions/deletions in the highly conserved overlaps between clones ANT32C12 and ANT8C10, and also between EBAC31A08 and EB000-45B06, are indicated. Differences in the lengths of homologous regions between the different clones are due to variations in the size of the orthologous genes. HOT2C01, HOT BAC clone that encodes a PR gene; EBAC31A08, Monterey Bay BAC clone that encodes both a PR gene and an rRNA operon; EB000-45B06, Monterey Bay BAC clone that overlaps EBAC31A08; ANT32C12, Antarctic fosmid clone that encodes a PR gene; ANT8C10, Antarctic fosmid clone that overlaps with ANT32C12; HOT-PR, HOT proteorhodopsin gene. (Scale bar = 10 kbp.)
Fig. 2.
Fig. 2.
Phylogenetic analysis of archaeal and bacterial rhodopsin family amino acid sequences. (Left) Phylogenetic analysis of PR, and archaeal [bacteriorhodopsin (BR), halorhodopsin (HR), and sensory rhodopsin (SR)], bacterial (Nostoc sp. PCC 7220), and eucaryal (Neurospora crassa, Leptosphaeria maculans, and Pyrocystis lunula) rhodopsin amino acid sequences. Minimal evolution inference method based on an analysis of 167 characters illustrates the relationship of the PR sequences to other rhodopsin sequences. Sequences indicated in bold represent PR sequences derived from the environmental genome fragments analyzed in this study. Bootstrap values, given as percentages from 1,000 replicate trees, are indicated for branches supported by >50% of the trees. Shown are SR groups 1 and 2, BR, and HR. Sequences used for the construction of this tree were derived from Halorubrum sodomense, Halobacterium salinarum, Haloarcula vallismortis, Natronomonas pharaonis, Halobacterium sp., Neurospora crassa, Leptosphaeria maculans, Nostoc PCC 7220, and Pyrocystis lunula. (Right) Phylogenetic analysis of 167 characters from selected PR amino acid sequences showing the detailed relationship among the three PR variants examined in this study (indicated in bold) and those previously reported (refs. –5). Bootstrap values for maximum parsimony (upper) and minimal evolution (lower) analysis, given as percentages from 1,000 replicate trees, are indicated for branches supported by >50% of the trees. Amino acid sequences for the rhodopsin genes from Nostoc sp. PCC 7220 and Pyrocystis lunula were used as the outgroup.
Fig. 3.
Fig. 3.
Phylogenetic analyses of ribosomal proteins and RNA polymerase genes indicate that HOT2C01 is derived from an α-proteobacterium. (Left) Maximum parsimony analysis of 13 concatemerized ribosomal protein sequences demonstrating the relationship of the HOT2C01-encoded sequences to other α-proteobacterial genes. Amino acid sequences for ribosomal proteins L1, L10, L11, L2, L22, L23, L3, L4, L7/L12, S10, S12, S3, and S7 from HOT2C01, the EBAC31A08/EB000-45B06 contig, and selected organisms from completed genome projects were aligned individually, masked to include only homologous residues, and then concatenated to create a single sequence with 2,427 characters. Bootstrap values, given as percentages from 1,000 replicate trees, are indicated for branches supported by >50% of the trees. Sequences from Bacillus subtilis, Treponema pallidum, and Nostoc PCC 7120 were used as outgroups. (Right) Maximum parsimony analysis of RNA polymerase subunit beta′ (RpoC) amino acid sequences indicates that HOT2C01 is derived from the genome of an unknown marine α-proteobacterium. Bootstrap values, given as percentages from 1,000 trees based on the resampling of 1,420 characters, are indicated for branches supported by >50% of the trees. Sequences from Bacillus subtilis, Treponema pallidum, and Nostoc PCC 7120 were used as outgroups.
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