The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Olsen, Jeanine L.; Rouzé, Pierre; Verhelst, Bram; Lin, Yao‐Cheng; Bayer, Till; Collén, Jonas; Dattolo, Emanuela; Paoli, Emanuele De; Dittami, Simon M.; Maumus, Florian; Michel, Gurvan; Kersting, Anna R.; Lauritano, Chiara; Lohaus, Rolf; Töpel, Mats; Tonon, Thierry; Vanneste, Kevin; Amirebrahimi, Mojgan; Brakel, Janina; Boström, Christoffer; Chovatia, Mansi; Grimwood, Jane; Jenkins, Jerry; Jueterbock, Alexander; Mraz, Amy; Stam, Wytze T.; Tice, Hope; Bornberg‐Bauer, Erich; Green, Pamela J.; Pearson, Gareth A.; Procaccini, Gabriele; Duarte, Carlos M.; Schmutz, Jeremy; Reusch, Thorsten B. H.; Peer, Yves Van de

doi:10.1038/nature16548

Cited by 448 publications

(547 citation statements)

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“…1c). Notably, Z. marina has lost genes for the production of volatile terpenes and lacks stomata on leaves (20), raising the possibility that seagrass leaves lack many of the characteristics of terrestrial plants (e.g., localized gas exchange via stomata, chemical defense, and communication) thought to influence the structure of their associated leaf microbiomes.…”

Section: Discussionmentioning

confidence: 99%

“…Seagrasses and their ecosystems have been the subject of a great amount of research covering topics including ecology and biogeography (48), evolution (49), physiology (19), and genetics (20). Here, we have provided a global-scale characterization of the microbial communities associated with Z. marina seagrasses by contrasting host samples with those of their surrounding environments across the entire Northern Hemisphere.…”

Section: Figmentioning

confidence: 99%

“…One widespread species, Zostera marina, or eelgrass, in particular, provides a habitat for ecologically diverse and economically important ecosystems along coasts throughout much of the Northern Hemisphere (16,17). The return of terrestrial seagrass ancestors to oceans is among the most severe habitat shifts accomplished by vascular plants (18) and has prompted detailed study of the physiological adaptations associated with this shift (19,20), including the tolerance of salinity and anoxic sediment conditions. Therefore, Z. marina is an ideal testbed for the study of microbial symbioses with plant hosts that uniquely exploit relatively harsh environments.…”

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Global-scale structure of the eelgrass microbiome

Fahimipour

Kardish

Eisen

et al. 2016

Preprint

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Plant-associated microorganisms are essential for their hosts' survival and performance. Yet, most plant microbiome studies to date have focused on terrestrial species sampled across relatively small spatial scales. Here, we report the results of a global-scale analysis of microbial communities associated with leaf and root surfaces of the marine eelgrass Zostera marina throughout its range in the Northern Hemisphere. By contrasting host microbiomes with those of surrounding seawater and sediment, we uncovered the structure, composition, and variability of microbial communities associated with eelgrass. We also investigated hypotheses about the assembly of the eelgrass microbiome using a metabolic modeling approach. Our results reveal leaf communities displaying high variability and spatial turnover that mirror their adjacent coastal seawater microbiomes. By contrast, roots showed relatively low compositional turnover and were distinct from surrounding sediment communities, a result driven by the enrichment of predicted sulfur-oxidizing bacterial taxa on root surfaces. Predictions from metabolic modeling of enriched taxa were consistent with a habitat-filtering community assembly mechanism whereby similarity in resource use drives taxonomic cooccurrence patterns on belowground, but not aboveground, host tissues. Our work provides evidence for a core eelgrass root microbiome with putative functional roles and highlights potentially disparate processes influencing microbial community assembly on different plant compartments.IMPORTANCE Plants depend critically on their associated microbiome, yet the structure of microbial communities found on marine plants remains poorly understood in comparison to that for terrestrial species. Seagrasses are the only flowering plants that live entirely in marine environments. The return of terrestrial seagrass ancestors to oceans is among the most extreme habitat shifts documented in plants, making them an ideal testbed for the study of microbial symbioses with plants that experience relatively harsh abiotic conditions. In this study, we report the results of a global sampling effort to extensively characterize the structure of microbial communities associated with the widespread seagrass species Zostera marina, or eelgrass, across its geographic range. Our results reveal major differences in the structure and composition of above-versus belowground microbial communities on eelgrass surfaces, as well as their relationships with the environment and host.

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Section: Discussionmentioning

confidence: 99%

Section: Figmentioning

confidence: 99%

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Global-scale structure of the eelgrass microbiome

Fahimipour

Kardish

Eisen

et al. 2016

Preprint

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“…Homologous carbohydrate sulfotransferases are indeed conserved at least in metazoans, brown algae, and red algae, so were most likely present in the last-common eukaryotic ancestor (91,93). Genes encoding carbohydrate sulfotransferases are not found in sequenced genomes of terrestrial plants and freshwater algae, but marine angiosperms have, relatively recently, readapted to the marine environment by developing an ECM containing sulfated polysaccharides through an unknown mechanism of convergent evolution (94). This speaks to the critical role of sulfated ECMs in high-salinity environments (physiological saline and seawater).…”

Section: Significancementioning

confidence: 99%

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Brawley¹,

Blouin²,

Ficko-Blean³

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Porphyra umbilicalis (laver) belongs to an ancient group of red algae (Bangiophyceae), is harvested for human food, and thrives in the harsh conditions of the upper intertidal zone. Here we present the 87.7-Mbp haploid Porphyra genome (65.8% G + C content, 13,125 gene loci) and elucidate traits that inform our understanding of the biology of red algae as one of the few multicellular eukaryotic lineages. Novel features of the Porphyra genome shared by other red algae relate to the cytoskeleton, calcium signaling, the cell cycle, and stress-tolerance mechanisms including photoprotection. Cytoskeletal motor proteins in Porphyra are restricted to a small set of kinesins that appear to be the only universal cytoskeletal motors within the red algae. Dynein motors are absent, and most red algae, including Porphyra, lack myosin. This surprisingly minimal cytoskeleton offers a potential explanation for why red algal cells and multicellular structures are more limited in size than in most multicellular lineages. Additional discoveries further relating to the stress tolerance of bangiophytes include ancestral enzymes for sulfation of the hydrophilic galactan-rich cell wall, evidence for mannan synthesis that originated before the divergence of green and red algae, and a high capacity for nutrient uptake. Our analyses provide a comprehensive understanding of the red algae, which are both commercially important and have played a major role in the evolution of other algal groups through secondary endosymbioses.cytoskeleton | calcium-signaling | carbohydrate-active enzymes | stress tolerance | vitamin B 12T he red algae are one of the founding groups of photosynthetic eukaryotes (Archaeplastida) and among the few multicellular lineages within Eukarya. A red algal plastid, acquired through secondary endosymbiosis, supports carbon fixation, fatty acid synthesis, and other metabolic needs in many other algal groups in ways that are consequential. For example, diatoms and haptophytes have strong biogeochemical effects; apicomplexans cause human disease (e.g., malaria); and dinoflagellates include both coral symbionts and toxin-producing "red tides" (1). The evolutionary processes that produced the Archaeplastida and secondary algal lineages remain under investigation (2-5), but it is clear that both nuclear and plastid genes from the ancestral red algae have contributed dramatically to broader eukaryotic evolution and diversity. Consequently, the imprint of red algal metabolism on the Earth's climate system, aquatic foodwebs, and

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“…Detection of genes that are missing only from the predicted gene space indicate that an optimization of the gene prediction algorithms is needed, since these tools frequently suffer from the lack of proper training in a newly sequenced organism. The absence of specific genes in the genome, and not just the assembly, should be independently confirmed using, for example, de novo assembled transcripts (Olsen et al, 2016) or hybridization-based molecular techniques.…”

Section: Conclusion and Guidelinesmentioning

confidence: 99%