Single-celled green algae, also known as green microalgae, play an important role for the world’s ecosystems, in part, because they can harness energy from sunlight to produce carbon-rich compounds. Microalgae are also important for biotechnology and people have harnessed them to make food, fuel and medicines. Green microalgae live in many types of habitats from streams to oceans, and they can also be found on the land, including in deserts. Like plants that live in the desert, these microalgae have likely evolved specific traits that allow them to live in these hot and dry regions. Yet, fewer scientists have studied microalgae compared to land plants, and until now it was not well understood how microalgae could survive in the desert.

Nelson et al. analyzed green microalgae from different locations around the United Arab Emirates and found that one microalga, known as Chloroidium, is one of the most dominant algae in this area. This included samples from beaches, mangroves, desert oases, buildings and public fresh water sources. Chloroidium has a unique set of genes and proteins and grew particularly well in freshwater and saltwater. Rather than just harnessing sunlight, the microalgae were able to consume over 40 different varieties of carbon sources to produce energy. The microalgae also accumulated oily molecules with a similar composition to palm oil, which may help this species to survive in desert regions.

A next step will be to develop biotechnological assets based on the information obtained. In the future, microalgae could be used to make an oil that represents an alternative to palm oil; this would reduce the demand for palm tree plantations, which pose a major threat to the natural environment. Moreover, understanding how microalgae can colonize a desert region will help us to understand the effects of climate change in the region.

Green algae play important ecological roles as primary biomass producers and are emerging as viable sources of commercial compounds in the food, fuel, and pharmaceutical industries. However, relatively few species of green algae have been characterized in depth at the genomic and metabolomic levels (Koussa et al., 2014; Salehi-Ashtiani et al., 2015; Chaiboonchoe et al., 2016). Also, recent genomics studies lack accompanying phenotype studies that could provide valuable context (Bochner, 2009; Chaiboonchoe et al., 2014). Analyses of this scope are necessary to better understand the ecology and physiology of microscopic algae (microphytes), both at the local and global scales, and to optimize their cultivation and yield of bioproducts for industrial applications (Abdrabu et al., 2016). Currently, species with superior growth characteristics for large-scale cultivation remain understudied, under-developed, and under-exploited (Fu et al., 2016).

Our study focuses on the green alga – formerly identified as Chloroidium sp. DN1 and accessioned at the Culture Collection of Algae at the University of Texas at Austin (UTEX) as Chloroidium sp. UTEX 3007, which we recently isolated in a screen for lipid-producing algae (Sharma et al., 2015). Its oleogenic properties, robust growth, and capacity to survive in a wide range of environmental conditions prompted us to carry out whole-genome sequencing and phenomic analyses. Genomic (Dataset 1) and phenomic (Dataset 2) datasets are available online at Dryad (Nelson et al., 2017).

We discovered that this species accumulates palmitic acid that, in conjunction with other traits, may enable its survival in a desert climate. The mechanisms employed by desert extremophiles such as Chloroidium sp. UTEX 3007 to maintain cellular integrity despite the oxidative insults of a desert climate may yield insight into the biology of a key player in a desert ecosystem and may also provide resources for the production of highly thermo-oxido-stable oils for human use.

One of the most important thermo-oxido-stable oils for human civilization is produced by the oil palm tree, Elaeis guineensisis (Barcelos et al., 2015). Palm oil’s distinguishing characteristics stem from its uniquely high concentrations of palmitic acid, which, due to its carbon chain length and lack of reactive double bonds, remains stable in conditions that destroy other longer and more unsaturated fatty acids. However, cultivation of trees for palm oil production has led to extensive destruction of high-biodiversity rainforests and wetlands that threatens to expand around the globe (Abrams et al., 2016). In addition to the loss of unique and diverse flora and fauna (Labrière et al., 2015; Wich et al., 2014), clear-cutting these regions for palm oil plantations has devastated major carbon sinks (Yue et al., 2015) and caused intensive production of smoke pollution that affects millions of people in densely populated areas (Bhardwaj et al., 2016; Vadrevu et al., 2014). Thus, an alternative source of palmitic acid could be valuable in terms of elevated product output, environmental preservation and a reduction of smoke pollution.

We re-isolated Chloroidium strains from diverse locations around the UAE including coastal beaches, mangroves, and inland desert oases (Figure 1a–b). The frequent re-isolation of the species from these different habitats suggests a broad habitat range in the local, predominantly desert, region. Due to its ubiquitous occurrence and lipid accumulation phenotype (Figure 1c), we selected Chloroidium sp. UTEX 3007 for study as a well-adapted species within the UAE and a potential candidate species of interest for production of oil replacement products (Sharma et al., 2015).

Figure 1

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Bioreactor growth

Chloroidium sp. UTEX 3007 reproduces via unequal autospores (2–8 cells/division); cells vary greatly in size from 1 to 12 μm in diameter (mean = 6 μm; Figure 2a) and exhibit ovoid morphology, parietal chloroplasts, and accumulation of prominent intracellular lipid deposits (Figures 1 and 2). Stationary phase is reached after ~2 weeks of growth in F/2 media (Figure 2). Chloroidium sp. UTEX 3007 showed robust growth in open pond simulators (OPSs), which generate a sinusoidal approximation of daily light based on geographical information system (GIS) data on daily light/dark cycles to simulate the growth conditions of an outdoor large-scale algae growth operation (Figure 2—figure supplement 1) (Lucker et al., 2014; Tamburic et al., 2014). We note that, because OPSs tend to underestimate growth rates compared to actual open ponds (Lucker et al., 2014; Tamburic et al., 2014), the actual productivity in an open pond may be higher. Under simulated parameters, growth occurs at 0–60 g/L NaCl and culture maturity (i.e., the transition from log to stationary phase) is reached after about two weeks (Figure 2b).

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Cell diameter measurements.

https://doi.org/10.7554/eLife.25783.005

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Figure 2—source data 2

Cell concentration time course measurements.

https://doi.org/10.7554/eLife.25783.006

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Figure 2—source data 3

Flow cytometry measurements.

https://doi.org/10.7554/eLife.25783.007

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Lipid accumulation

Upon entering stationary phase, lipid accumulation commences and causes an increase in size, weight (2-6x, ~100–200 pg/cell dry weight), and relative fluorescence of lipophilic dye stained cells (Figures 1 and 2). After reaching stationary phase, Chloroidium sp. UTEX 3007 cultures remain stable and continue to increase biomass at a reduced rate (Figure 2b).

Our results indicate that the slowly accruing biomass in post-stationary phase is concurrent with an accumulation of triacylglycerols (TAGs) composed of mostly palmitic acid side-chains (Figure 3a). The presence of palmitic acid instead of other longer and more unsaturated fatty acids is expected to increase fitness at higher temperatures because palmitic acid is more thermostable.

Figure 3

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GC-FID results for major fatty acid species in Chloroidium sp. UTEX 3007.

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Figure 3—source data 2

Fatty acid profiles of Chloroidium sp. UTEX 3007, Elaeis guineensis (Barcelos et al., 2015), and several other algal isolates (Lang et al., 2011).

https://doi.org/10.7554/eLife.25783.012

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HPLC-MS base peak chromatograms (BPCs) for Chloroidium sp. UTEX 3007 and Chlamydomonas reinhardtii extracts.

https://doi.org/10.7554/eLife.25783.013

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Metabolic requirements

To define the spectrum of nutrients and metabolites that support heterotrophic growth, we exposed the strain to hundreds of chemical compounds in phenotype microarray plates (Figure 4a, Dataset 2). This method has been used successfully to identify new compounds that support heterotrophic growth in the model green alga Chlamydomonas reinhardtii (Chaiboonchoe et al., 2014). Chloroidium sp. UTEX 3007 grew on more than 40 different carbon sources, including several desiccation-promoting sugars including trehalose, sorbitol, raffinose, and palatinose (Dataset 2).

Figure 4

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Phenotype microarray results for plates PM1, PM2, and PM3.

https://doi.org/10.7554/eLife.25783.015

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Figure 4—source data 2

GC-MS results for Chloroidium sp. UTEX 3007 (Cm) and Chlamydomonas reinhardtii (Cre) intracellular polar metabolites.

https://doi.org/10.7554/eLife.25783.016

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Although Chloroidium species have been documented to accumulate the pentose ribitol, to date, no green alga has been shown to use a pentose sugar (for example arabitol and lyxose, which Chloroidium sp. UTEX 3007 can assimilate) for heterotrophic growth. Thus, our experiments show that some green algae have a wider range of sugar utilization than previously recognized. Because Chloroidium sp. UTEX 3007 was able to use common plant polysaccharides and sugars, including cellulose, fructose, and fucose for heterotrophic growth (Figure 4), our nutrient assays suggest a herbivoric capacity for the Chloroidium species. Strikingly, growth on L-glucose was also observed in our assays.

In contrast to Chlamydomonas reinhardtii, which can only use acetate as a carbon source for heterotrophic growth, Chloroidium sp. UTEX 3007 lacked the capacity to assimilate extracellular acetate for growth. We found that a different profile of nitrogen sources supports growth in Chloroidium sp. UTEX 3007 in comparison with Chlamydomonas reinhardtii. Although Chlamydomonas reinhardtii can use a broad range of nitrogen sources, including several D-amino acids (Chaiboonchoe et al., 2014), major nitrogen sources promoting growth of Chloroidium sp. UTEX 3007 were limited to ammonium, nitrate, urea, agmatine, ornithine, and glutamine (Figure 4a). These differences in nutrient assimilatory capacities might reflect differences in the habitats of the two algae, such as the composition of the soil or other species in their immediate vicinity. A desert environment may offer only limited nitrogen sources, while the fertile soil of typical Chlamydomonas reinhardtii habitats, that is, the temperate climate zone, often contains a wide variety of nitrogen sources (Harris, 2009).

In addition to GC-FID and HPLC-MS, we also performed metabolite profiling using GC-MS to examine other simple carbon and nitrogen compounds in Chloroidium sp. UTEX 3007 and Chlamydomonas reinhardtii. While Chloroidium sp. UTEX 3007 accumulated a wide assortment of sugars, a much broader range of nitrogen metabolites was accumulated by Chlamydomonas reinhardtii (Figure 4b). These results complement the phenotype microarray results. Carbon compounds accumulated by Chloroidium sp. UTEX 3007 include the desiccation resistance-promoting sugars arabitol, ribitol, and trehalose (Figure 4b). Based on previous findings, (Santacruz-Calvo et al., 2013; Watanabe et al., 2016), these sugars and lipids are likely to be involved in osmotic stabilization in C. sp. UTEX 3007.

Genome-scale metabolic network reconstruction and oil accumulation pathways

From our functional annotation of Chloroidium sp. UTEX 3007’s genome, we reconstructed a genome-scale metabolic pathway model by mapping predicted genes to metabolic network nodes reconstructed from pathways in the BioCyc database (https://biocyc.org/). The model can be found in Dataset 1. Our metabolic model highlights known pathways of potential lipid biosynthesis in Chloroidium sp. UTEX 3007. This analysis also revealed unusual lipid biosynthesis mechanisms including TAG biosynthesis from membrane lipids instead of an acyl-CoA pool. This has previously been documented in some yeast and plant species that use phospholipids as acyl donors and diacylglycerol as the acceptor (Cases et al., 2001; Dahlqvist et al., 2000).

To investigate possible pathways in Chloroidium sp. UTEX 3007 that could synthesize TAGs from polar membrane lipids, we examined enzymes with phospholipid-cleaving or phospholipid-translocating activities. Our BLASTP/BLAST2GO analyses highlighted an abundance of phospholipid-translocating ATPases that might be involved in this process (Dataset 1). From our protein family domain analysis, we detected lecithin retinol acyltransferase (LRAT) and phospholipase D (PLD) domain-containing enzymes in Chloroidium sp. UTEX 3007 (Figure 5) that are also candidate proteins for rapidly modifying membrane lipids (Dataset 1). Membrane-bound LRAT enzymes are involved in the transfer of palmitoyl groups to and from a variety of biomolecules (Furuyoshi et al., 1993; Golczak and Palczewski, 2010), and several phospholipases, including those from the PLD family, cleave phosphate groups from membrane lipids. One predicted PLD in Chloroidium sp. UTEX 3007 contains several C2 calcium-binding domains, indicating that it acts on membrane phospholipids to produce membrane-bound phosphatidic acid (PA) and cytosolic choline (Rahier et al., 2016). PA has noted roles in environmental stress response (Peppino Margutti et al., 2017), and its liberation has been shown to create ‘supersized’ lipid droplets (Fei et al., 2011). We hypothesize that phospholipases acting on membrane lipids could play particularly important roles in osmotic stress resistance and lipid accumulation in Chloroidium sp. UTEX 3007 as they represent a key branch point between polar and non-polar lipid species.

Figure 5

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Locations, confidence scores, and accession numbers for PLD and C2 Pfam domains in Chloroidium sp. UTEX 3007.

https://doi.org/10.7554/eLife.25783.018

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Unique protein families

We sought to compare and contrast Chloroidium sp. UTEX 3007’s genome with other species from diverse clades within the green algae. Our approach compares the euryhaline Chloroidium sp. UTEX 3007 with salt- and fresh-water-dwelling species and highlights Pfam domains that are unique to Chloroidium sp. UTEX 3007. The genomes of Chlorella variabilis NC64A (Blanc et al., 2010), Micromonas pusilla (Worden et al., 2009), Ostreococcus tauri (Blanc-Mathieu et al., 2014), and Coccomyxa subellipsoidea (Blanc et al., 2012) were downloaded from the National Center for Biotechnology Information (NCBI), and the Chlamydomonas reinhardtii genome (Merchant et al., 2007) was downloaded from Phytozome (v5.5; www.phytozome.net). De novo gene prediction using an A. thaliana HMM in SNAP yielded a set of peptide predictions (Dataset 1) that served as a base for HMM alignment with Pfam-A (v31.0, (http://hmmer.org)).

Figure 6 provides a graphical representation of unique and shared Pfam domains among the six algal species in an interactive Venn diagram (Figure 5—source data 1) using InteractiVenn (http://www.interactivenn.net/)(Heberle et al., 2015). Chlorella sp. NC64A contained the lowest number of unique Pfam domains (174), while, surprisingly, Ostreococcus tauri, known for its minimal genome, had the highest number of unique Pfams (427).

Figure 6

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Predicted Pfam designations for each species in Figure 6.

https://doi.org/10.7554/eLife.25783.020

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Figure 6—source data 2

Table with QUAST results used in (b).

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Figure 6—source data 3

Interactive Venn diagram that can be viewed at interactivenn.net to obtain Pfam sets for numbers displayed in Figure 6.

https://doi.org/10.7554/eLife.25783.022

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In comparison with other algae, we found 235 Pfam domains that were unique to Chloroidium sp. UTEX 3007 and may play roles in its inhabitation of a desert region. Selected, unique, Pfam entries with relevance to phenotypes documented in this manuscript and unique to Chloroidium sp. UTEX 3007 are shown in Table 1. For example, the detection of a NST1 domain suggests the presence of proteins involved in cellular response to hypo-osmolarity (Leng and Song, 2016). Similarly, the presence of a proline-rich domain is associated with thermotolerance (Cvikrová et al., 2012; Khan et al., 2013). In all other cases for the abiotic stress column, oxidative stress resistance, either direct or metal-mediated, is suggested. Because mechanisms to deal with oxidative stress from a variety of sources (sun, salt, drought, heat) are necessary to survive in a desert climate, gene products encoded with these domains may play a key role in the successful colonization of a desert region, and its various sub-habitats, by Chloroidium sp. UTEX 3007.

Table 1

	Description	Key	i-Evalue
(a)	Iron-containing redox enzyme	Haem_oxygenas_2	7.50E-05
	Salt tolerance down-regulator	NST1	0.00012
	Proline-rich	Pro-rich	0.00015
	Peroxisome biogenesis factor	PEX-2N	0.003
	OsmC-like protein	OsmC	0.0066
	NA,K-Atpase interacting protein	NKAIN	0.003
	Metallothionein	Metallothio_2	0.0074
	Mercuric transport protein	MerT	0.0054
(b)	Beta-galactosidase jelly roll domain	BetaGal_dom4_5	0.013
	Cryptococcal mannosyltransferase	CAP59_mtransfer	3.50E-15
	Carbohydrate binding domain CBM49	CBM49	0.0085
	Carbohydrate binding domain (family 25)	CBM_25	0.0023
	Carbohydrate binding domain	CBM_4_9	0.00036
	Cellulose biosynthesis protein BcsN	CBP_BcsN	0.0018
	Glycosyl hydrolase family 70	Glyco_hydro_70	0.00054
	Glycosyl hydrolase family 9 (heptosyltransferase)	Glyco_transf_9	0.0025
	Carbohydrate esterase/acetylesterase	SASA	2.00E-06
	Activator of aromatic catabolism	XylR_N	0.011

Manganese catalase-like genes

BLAST2GO analysis revealed that Chloroidium sp. UTEX 3007 contains a disproportionately high number of genes involved in redox chemistry and metal binding (Dataset 1) Exploring these genes further with functional and phylogenetic analyses highlighted a cluster of genes (CDS1/2/3) with homologs in desiccation-associated proteins from Deinococcus species (Figure 7, Figure 7—figure supplement 1).

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Models of CDS1-3 in protein data bank (PDB) format.

https://doi.org/10.7554/eLife.25783.025

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Figure 7—source data 2

Amino acid residue alignment of CDS1-3.

https://doi.org/10.7554/eLife.25783.026

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The proteins from (CDS1/2/3) contain ferritin-like domains and may be involved in neutralizing reactive oxygen species (ROS) via manganese redox cycles (Daly, 2009; Fredrickson et al., 2008). Consistent with the primary sequence analysis, homology-based tertiary structure modeling confirmed that these proteins contain the metal binding motifs and extended C-terminal tails characteristic of manganese (Mn) catalases (Whittaker, 2012) (Figure 7). As intracellular iron can become toxic in the face of overwhelming oxidative stress from changing environments, the utilization of manganese as a replacement would offer a protective advantage in the face of severe oxidative stress (Daly, 2009; Fredrickson et al., 2008).

Algal genomes are under-represented among sequenced organisms (Grossman et al., 2010; Umen and Olson, 2012), and genome-scale studies fully incorporating metabolomics are, in general, poorly represented within the scientific literature (Chaiboonchoe et al., 2014). As microphytic species play fundamental roles in maintaining nutrient flow through ecosystems (Akhter et al., 2016), the study of their genomic and phenotypic characteristics is critical to fully understand local and global ecosystem dynamics. Our analysis provides a detailed genome-phenome description of a green alga from a desert area and reveals insight into traits that could facilitate acclimatization to this climate.

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Author details

1. David R Nelson

   1. Laboratory of Algal, Synthetic, and Systems Biology, Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates
   2. Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   DRN, Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Methodology, Writing—original draft, Project administration

   For correspondence

   drn2@nyu.edu

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0001-8868-5734

2. Basel Khraiwesh

   1. Laboratory of Algal, Synthetic, and Systems Biology, Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates
   2. Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   BK, Conceptualization, Supervision, Methodology, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0001-7026-1263

3. Weiqi Fu

   Laboratory of Algal, Synthetic, and Systems Biology, Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   WF, Conceptualization, Formal analysis, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-7368-383X

4. Saleh Alseekh

   Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany

   Contribution

   SA, Formal analysis, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0003-2067-5235

5. Ashish Jaiswal

   Laboratory of Algal, Synthetic, and Systems Biology, Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   AJ, Conceptualization, Software, Formal analysis, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-6193-1824

6. Amphun Chaiboonchoe

   Laboratory of Algal, Synthetic, and Systems Biology, Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   AC, Data curation, Software, Formal analysis, Visualization, Methodology, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-0009-0806

7. Khaled M Hazzouri

   Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   KMH, Conceptualization, Software, Formal analysis, Investigation, Methodology, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

8. Matthew J O’Connor

   Core Technology Platform, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   MJO’C, Conceptualization, Resources, Data curation, Software, Formal analysis, Methodology

   Competing interests

   The authors declare that no competing interests exist.

9. Glenn L Butterfoss

   Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

   Contribution

   GLB, Conceptualization, Data curation, Software, Formal analysis, Investigation, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

10. Nizar Drou

    Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

    Contribution

    ND, Conceptualization, Data curation, Software, Formal analysis, Investigation, Methodology, Writing—review and editing

    Competing interests

    The authors declare that no competing interests exist.

11. Jillian D Rowe

    Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

    Contribution

    JDR, Conceptualization, Data curation, Software, Methodology

    Competing interests

    The authors declare that no competing interests exist.

12. Jamil Harb

    1. Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    2. Department of Biology and Biochemistry, Birzeit University, Birzeit, Palestine

    Contribution

    JH, Conceptualization, Resources, Supervision, Investigation, Methodology, Project administration

    Competing interests

    The authors declare that no competing interests exist.

    "This ORCID iD identifies the author of this article:" 0000-0001-6334-3746

13. Alisdair R Fernie

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany

    Contribution

    ARF, Conceptualization, Resources, Formal analysis, Supervision, Validation, Investigation, Methodology, Project administration, Writing—review and editing

    Competing interests

    The authors declare that no competing interests exist.

14. Kristin C Gunsalus

    1. Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates
    2. Center for Genomics and Systems Biology and Department of Biology, New York University, New York, United States

    Contribution

    KCG, Resources, Supervision, Funding acquisition, Investigation, Methodology, Project administration, Writing—review and editing

    Competing interests

    The authors declare that no competing interests exist.

15. Kourosh Salehi-Ashtiani

    1. Laboratory of Algal, Synthetic, and Systems Biology, Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates
    2. Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

    Contribution

    KS-A, Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

    For correspondence

    ksa3@nyu.edu

    Competing interests

    The authors declare that no competing interests exist.

    "This ORCID iD identifies the author of this article:" 0000-0002-6521-5243

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