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Xenorhodopsins, an Enigmatic New Class of Microbial Rhodopsins Horizontally Transferred Between Archaea and Bacteria

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Xenorhodopsins, an Enigmatic New Class of Microbial Rhodopsins Horizontally Transferred Between Archaea and Bacteria UC San Diego UC San Diego Previously Published Works Title Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between Archaea and Bacteria Permalink https://escholarship.org/uc/item/8rg5f54b Journal Biology Direct, 6(1) ISSN 1745-6150 Authors Ugalde, Juan A Podell, Sheila Narasingarao, Priya et al. Publication Date 2011-10-10 DOI http://dx.doi.org/10.1186/1745-6150-6-52 Supplemental Material https://escholarship.org/uc/item/8rg5f54b#supplemental Peer reviewed eScholarship.org Powered by the California Digital Library University of California Ugalde et al. Biology Direct 2011, 6:52 http://www.biology-direct.com/content/6/1/52 DISCOVERYNOTES Open Access Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria Juan A Ugalde1, Sheila Podell1, Priya Narasingarao1 and Eric E Allen1,2* Abstract Based on unique, coherent properties of phylogenetic analysis, key amino acid substitutions and structural modeling, we have identified a new class of unusual microbial rhodopsins related to the Anabaena sensory rhodopsin (ASR) protein, including multiple homologs not previously recognized. We propose the name xenorhodopsin for this class, reflecting a taxonomically diverse membership spanning five different Bacterial phyla as well as the Euryarchaeotal class Nanohaloarchaea. The patchy phylogenetic distribution of xenorhodopsin homologs is consistent with historical dissemination through horizontal gene transfer. Shared characteristics of xenorhodopsin-containing microbes include the absence of flagellar motility and isolation from high light habitats. Reviewers: This article was reviewed by Dr. Michael Galperin and Dr. Rob Knight. Findings disseminated photoreceptor and photosensory activities Microbial rhodopsins are a widespread family of photo- across large evolutionary distances [1]. One salient active proteins found in all three domains of life. Based example is a putative sensory rhodopsin found in the on their functional roles, characterized rhodopsin pro- bacterium Anabaena (Nostoc) sp. PCC 7120 (Anabaena teins have been classified into three distinct groups: (i) sensory rhodopsin, ASR). It has been suggested that this Proton pumps (bacteriorhodopsins and proteorhodop- protein was originally acquired from a halophilic sins), involved in energy generation, (ii) Chloride pumps archaeon by HGT, and may play a sensory role [1,2]. (halorhodopsins), involved in the maintenance of osmo- However, sensory function performance has not yet tic balance, and (iii) Sensory rhodopsins, which direct been demonstrated experimentally, and the ASR protein positive and/or negative phototaxis. Microbial proton differs from previously described sensory rhodopsins in: pumps have the widest ecological niche distribution, (i) a distinct signaling cascade mechanism that employs and are found throughout the Bacteria and Archaea in a soluble transducer protein, rather than the methyl- hypersaline, marine, and freshwater habitats [1]. Chlor- accepting taxis transducers (HTR proteins) found in ide pumps and sensory rhodopsins are mostly limited to halophilic Archaea [2,5] and (ii) its divergent photo- halophilic Archaea of class Halobacteria [1], excepting chemistry, including unique light-induced cis/trans con- the few characterized examples in the freshwater cyano- figuration dynamics of the retinal chromophore, bacterium Anabaena (Nostoc) sp. PCC 7120 [2,3] and providing a possible mechanism for sensing and differ- eukaryotic green algae including Chlamydomonas rein- entiating specific light qualities [3,6]. hardtii [4]. In the current study, we report the discovery of sev- The evolutionary history of microbial rhodopsins is eral new ASR protein homologs with shared characteris- complex, showing broad but patchy phylogenetic distri- tics consistent with the designation of a new class of bution within and across disparate lineages. It has been microbial rhodopsins. ASR homologs were found in suggested that horizontal gene transfer (HGT) has Nanosalina sp. J07AB43 and Nanosalinarum sp. J07AB56, the first representatives of a newly described * Correspondence: [email protected] major lineage of Archaea (class Nanohaloarchaea) within 1 Marine Biology Research Division, Scripps Institution of Oceanography, phylum Euryarchaeota [7]. The Nanosalina sp. and University of California, San Diego, La Jolla, CA 92093-0202, USA Full list of author information is available at the end of the article Nanosalinarum sp. rhodopsin proteins are highly similar © 2011 Ugalde et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Ugalde et al. Biology Direct 2011, 6:52 Page 2 of 8 http://www.biology-direct.com/content/6/1/52 to each other (89% amino acid identity) and are present protein sequences from all previously recognized func- in both genomes as single copy genes. Surprisingly, tional microbial rhodopsin classes. Methods and experi- these two Nanohaloarchaeal proteins most closely mental procedures are provided in Additional File 1. resemble rhodopsins in taxonomically distant Cya- The phylogenetic tree also includes additional sequences nothece sp. PCC 7424 and Anabaena (Nostoc)sp.PCC we obtained by PCR amplification using primers specifi- 7120, at 31 and 34% amino acid identity respectively. cally targeting Nanohaloarchaeal rhodopsin genes. These No homologs were identified in other members of the sequences were recovered from a hypersaline environ- Euryarchaeota, although related proteins were detected ment (South Bay Salt Works, Chula Vista, California, at 30-31% amino acid identity in Bacillus coahuilensis USA) that is geographically distant from the original iso- m4-4 (phylum Firmicutes), a sporulating halophilic bac- lation site of the Nanohaloarchaea genomes (Lake Tyr- terium isolated from a desiccation lagoon [8], the psy- rell, Victoria, Australia). Tree topology shows robust chrophilic bacterium Hymenobacter roseosalivarius AA- clustering of all ASR homologs as a single clade, distinct 718 (phylum Bacteroidetes), and the halophilic bacter- from other rhodopsin types. We propose the name ium Haloplasma contractile SSD-17B (phylum Teneri- “xenorhodopsins” to describe this class of rhodopsin cutes) [9,10]. proteins, articulating the wide taxonomic diversity of its Figure 1 shows a phylogenetic analysis using maxi- members. mum likelihood and Bayesian inference methods for the The patchy distribution and topology of the xenorho- ASR homologs, together with a set of representative dopsin clade is consistent with HGT events between Hymenobacter roseosalivarius (IMG_2502504230) 100/100 Anabaena (Nostoc) sp. PCC 7120 [ASR] (NP_487205) 100/100 Cyanothece sp. PCC 7424 (YP_002379171.1) 57/- 99/94 Bacillus coahuilensis (ZP_03226327.1,ZP_03226326.1) 89/70 Haloplasma contractile SSD-17B (ZP_08554533.1) Xenorhodopsin Nanosalinarum sp. (EGQ40596.1) 100/100 CV1 (JN603996) 99/98 87/83 CV2 (JN603997) Nanosalina sp. (EGQ43296.1) 100/99 Haloarcula valiismortis (P94854.1) 84/- Haloarcula marismortui [1] (YP_137573.1) 100/100 Haloarcula marismortui [2] (YP_136594.1) Bacteriodetes (Bac) 92/60 100/99 Bacteriorhodopsin Haloquadratum walsbyi [1] (YP_656801.1) Cyanobacteria (Bac) 55/- Firmicutes (Bac) Halobacterium salinarum (YP_001689404.1) Tenericutes (Bac) Haloquadratum walsbyi [2] (YP_656804.1) 52/50 Euryarchaeota (Arc) Salinibacter ruber (YP_446872.1) 100/100 Natronomonas pharaonis (YP_325981.1) 88/- Haloarcula marismortui (YP_136278.1) 100/94 Halorhodopsin 97/73 Haloarcula valiismortis (P94853.1) 99/92 Haloquadratum walsbyi (YP_658762.1) 51/- Halobacterium salinarum (YP_001688407.1) Salinibacter ruber (YP_446609.1) 100/99 Salinibacter ruber (YP_446677.1) 100/100 Sensory Halobacterium salinarum (YP_001689548.1) 100/99 Type I 80/70 100/98 Haloarcula valiismortis (Q48334.1) Haloarcula marismortui (YP_137680.1) 100/79 Haloarcula marismortui [SRM] (YP_135281.1) Sensory Type III Halobacterium salinarum (YP_001689625.1) 98/67 Haloarcula valiismortis (CAA84550.1) 100/100 Sensory 100/75 Haloarcula marismortui (YP_134805.1) Type II Natronomonas pharaonis (YP_331142.1) 100/100 Proteorhodopsin 0.3 Figure 1 Phylogenetic tree of microbial rhodopsin proteins showing diversity of functional classes. Tree is based on a total of 34 sequences (205 amino acid positions) using maximum likelihood and Bayesian inference methods. Numbers at nodes represent posterior probablities inferred by MrBayes (first value) and maximum likelihood bootstrap values using RaxML (second value). Only values greater than 50% are shown. GenBank accession numbers are shown in parentheses for each protein except H. roseosalivarus (IMG-ER database gene object ID) [22]. Sequences CV1 and CV2 were recovered by PCR amplification of environmental DNA from a solar saltern in Chula Vista, California, USA, using Nanohaloarchaeal-specific xenorhodopsin primers (see Additional File 1). Ugalde et al. Biology Direct 2011, 6:52 Page 3 of 8 http://www.biology-direct.com/content/6/1/52 domains and involving five disparate bacterial phyla. The phylogenetic tree presented in Figure 1 includes The large numbers of currently sequenced Firmicute only known, modern representatives of lineages that (873), Bacteriodetes (169), Cyanobacteria (68), and may have incorporated multiple HGT events between Haloarchaea
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