The Evolution of Silicon Transporters in Diatoms1
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CORE Metadata, citation and similar papers at core.ac.uk Provided by Woods Hole Open Access Server J. Phycol. 52, 716–731 (2016) © 2016 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. DOI: 10.1111/jpy.12441 THE EVOLUTION OF SILICON TRANSPORTERS IN DIATOMS1 Colleen A. Durkin3 Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing California 95039, USA Julie A. Koester Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington North Carolina 28403, USA Sara J. Bender2 Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole Massachusetts 02543, USA and E. Virginia Armbrust School of Oceanography, University of Washington, Seattle Washington 98195, USA Diatoms are highly productive single-celled algae perhaps their dominant ability to take up silicic acid that form an intricately patterned silica cell wall after from seawater in diverse environmental conditions. every cell division. They take up and utilize silicic Key index words: diatoms; gene family; molecular acid from seawater via silicon transporter (SIT) evolution; nutrients; silicon; transporter proteins. This study examined the evolution of the SIT gene family to identify potential genetic Abbreviations: BLAST, Basic Local Alignment Search adaptations that enable diatoms to thrive in the Tool; GeoMICS, Global-scale Microbial Interactions modern ocean. By searching for sequence homologs across Chemical Survey; HMM, Hidden Markov in available databases, the diversity of organisms Model; JGI, Joint Genome Institute; MMETSP, Mar- found to encode SITs increased substantially and ine Microbial Eukaryotic Transcriptome Sequencing included all major diatom lineages and other algal Project; NCBI, National Center for Biotechnology protists. A bacterial-encoded gene with homology to Information; PCA, principal component analysis; SIT sequences was also identified, suggesting that a SAR, stramenopiles alveolates rhizaria; SIT, silicon lateral gene transfer event occurred between bacterial transporter; TM, transmembrane and protist lineages. In diatoms, the SIT genes diverged and diversified to produce five distinct Many organisms utilize silicon in some capacity; it clades. The most basal SIT clades were widely is required for bone formation in animals and the distributed across diatom lineages, while the more creation of siliceous structures in a wide variety of derived clades were lineage-specific, which together plants, algae, protists, and sponges (Simpson and Vol- produced a distinct repertoire of SIT types among cani 1981). The silica cell walls (frustules) produced major diatom lineages. Differences in the predicted by diatoms give these single-celled algae a distinct protein functional domains encoded among SIT and influential role in the ecology and biogeochem- clades suggest that the divergence of clades resulted istry of the oceans. Diatom silicification links the mar- in functional diversification among SITs. Both ine carbon and silicon cycles: diatoms are among the laboratory cultures and natural communities changed most productive organisms on earth, responsible for transcription of each SIT clade in response to an estimated 20% of global primary production, and experimental or environmental growth conditions, a corresponding 240 Tmol of biogenic silica precipi- with distinct transcriptional patterns observed among tation annually (Nelson et al. 1995). Diatoms are also clades. Together, these data suggest that the among the most diverse phytoplankton groups in the diversification of SITs within diatoms led to ocean, with over 20,000 described species (Round specialized adaptations among diatoms lineages, and and Crawford 1990, Julius 2007) that are most fre- quently identifiable by distinct silica frustule mor- phologies. The utilization of silicon by diatoms 1Received 19 January 2016. Accepted 21 May 2016. therefore appears to be strongly linked to their evolu- 2Present address: The Gordon and Betty Moore Foundation, Palo tion and has resulted in a unique ecological and bio- Alto, California 94304, USA. geochemical role for diatoms in the ocean. 3Author for correspondence: e-mail [email protected]. The copyright line for this article was changed on 14 October Silicon, in the form of silicic acid, is transported 2016 after original online publication. into the diatom cell from seawater by silicon trans- Editorial Responsibility: P. Kroth (Associate Editor) porter (SIT) proteins (Hildebrand et al. 1997, 716 SILICON TRANSPORTER EVOLUTION 717 Curnow et al. 2012, Shrestha and Hildebrand 2015). had the ability to actively transport silicic acid across SITs were first identified by Hildebrand et al. cell membranes even in a diffusion-mediated envi- (1997) in the pennate diatom Cylindrotheca fusiformis ronment. It is unclear what adaptive advantage SITs Reimann & J.C.Lewin and were soon thereafter rec- may have provided in early diatoms, whereas in ognized to be encoded by a multi-copy gene family modern oceans, SITs enable diatoms to utilize silicic (Hildebrand et al. 1998). Hildebrand et al. (1998) acid at reduced concentrations. hypothesized that the SIT proteins encoded by this Diatom cells respond to changes in silicic acid gene family play different roles in the uptake of sili- availability and environmental conditions in part by cic acid with different cellular localizations, Si bind- altering the expression of SIT genes and proteins. ing affinities, and transport rates. Early phylogenies SIT homologs encoded by laboratory isolates are dif- of SIT genes generally reflected the phylogeny of ferentially transcribed across the cell cycle and in diatom species, although discrepancies were noted response to silicic acid starvation, suggesting that (Thamatrakoln et al. 2006). As additional diatom homologs evolved different functions (Thama- sequences became available, a pattern of clade trakoln and Hildebrand 2007, Mock et al. 2008, divergence became evident: gene homologs were Sapriel et al. 2009, Durkin et al. 2012, Shrestha and identified among species and paralogs identified Hildebrand 2015). Notably, the abundance of SIT within species (Durkin et al. 2012). Five distinct transcripts and proteins are not correlated, indicat- clades were distinguished and named A through E. ing that they are subject to multiple levels of regula- The SIT genes encoded by diatoms are not homolo- tion (Thamatrakoln and Hildebrand 2007, Shrestha gous to the silicon transporters in sponges (sodium and Hildebrand 2015). Even so, the large variation bicarbonate symporters) or plants (aquaporins and in SIT transcript abundance often observed in cul- efflux transporters; Schroder€ et al. 2004, Ma et al. tures and in natural communities has been used as 2006, 2007), suggesting that SITs are a distinctly an indicator of a cellular response to conditions algal adaptation. affecting silicon-related processes. Durkin et al. Diatoms are stramenopiles and belong to the SAR (2012) observed changes in the transcription of SIT supergroup of protists (stramenopiles, alveolates, gene clades in natural communities that were attrib- and rhizaria; Sorhannus 2007, Adl et al. 2012). Sili- uted to nutrient availability and community compo- cification occurs in all three SAR clades, but is not sition. However, the limited reference phylogeny the rule (Preisig 1994). Moreover, silica precipita- could not resolve the species-specific responses. tion also occurs in the haptophytes (Yoshida et al. Here, current knowledge about SIT proteins is 2006), an algal lineage phylogenetically distinct placed within an evolutionary context to better char- from the SAR group. Among these algal lineages, acterize how SITs may influence present-day ecology SIT genes were identified in silicifying stramenopiles and biogeochemistry. We use large-scale sequence (chrysophytes and diatoms) and more recently in searches as well as gene expression, phylogenetic, haptophytes (Likhoshway et al. 2006, Durak et al. and metatranscriptome analyses to propose a model 2016). It is unclear whether the precipitation of sil- for SIT evolution in phytoplankton. The continued ica has a common origin among these algal lineages diversification of these proteins within diatoms has or whether the trait evolved independently among potentially led to specialized adaptations among dia- diverged lineages. The evolutionary history and tom lineages and perhaps their dominant ability to diversification of diatom SIT genes may help take up silicic acid from seawater in diverse environ- explain how diatoms became the dominant silicify- mental conditions. ing algae in the modern ocean. Diatom frustules first appeared in the fossil record 140 million years ago (Gersonde and Har- METHODS wood 1990) when the hypothesized concentration l Identification of transcribed, full-length SIT sequences. Gene of silicic acid in the ocean was around 1,000 M, models previously predicted to encode SITs were verified or orders of magnitude greater than that found in extended for sequences encoded by Thalassiosira pseudonana today’s oceans (Siever 1991, Treguer et al. 1995, Hasle & Heimdal, Pseudo-nitzschia multiseries Hasle, and Fragi- Maldonado et al. 1999). At concentrations