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. 2016 Oct 12;283(1840):20161455.
doi: 10.1098/rspb.2016.1455.

Genetic basis of priority effects: insights from nectar yeast

Manpreet K Dhami  1 , Thomas Hartwig  2 , Tadashi Fukami  3
Affiliations

Genetic basis of priority effects: insights from nectar yeast

Manpreet K Dhami et al. Proc Biol Sci. .

Abstract

Priority effects, in which the order of species arrival dictates community assembly, can have a major influence on species diversity, but the genetic basis of priority effects remains unknown. Here, we suggest that nitrogen scavenging genes previously considered responsible for starvation avoidance may drive priority effects by causing rapid resource depletion. Using single-molecule sequencing, we de novo assembled the genome of the nectar-colonizing yeast, Metschnikowia reukaufii, across eight scaffolds and complete mitochondrion, with gap-free coverage over gene spaces. We found a high rate of tandem gene duplication in this genome, enriched for nitrogen metabolism and transport. Both high-capacity amino acid importers, GAP1 and PUT4, present as tandem gene arrays, were highly expressed in synthetic nectar and regulated by the availability and quality of amino acids. In experiments with competitive nectar yeast, Candida rancensis, amino acid addition alleviated suppression of C. rancensis by early arrival of M. reukaufii, corroborating that amino acid scavenging may contribute to priority effects. Because niche pre-emption via rapid resource depletion may underlie priority effects in a broad range of microbial, plant and animal communities, nutrient scavenging genes like the ones we considered here may be broadly relevant to understanding priority effects.

Keywords: community assembly; competition; resource pre-emption; species interaction; tandem gene duplication.

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Figures

Figure 1.
Figure 1.
Genome of Metschnikowia reukaufii. (a) Flower of host plant sticky monkeyflower (M. aurantiacus), zoomed inset, scanning electron micrograph of M. reukaufii cells (blue) attached to cells and trichome of sticky monkeyflower floral tube that contains nectar (gold), Scale bar, 5 µm, false-coloured (b) CEGMA completion of M. reukaufii (Mreu, this study), compared to published yeast genomes, from nectar specialists (yellow: S. bombicola (Sbom), H. valbyensis (Hval), Metschnikowiaceace species (green: M. bicuspidata (Mbic), Cl. lusitaniae (Clus)) and closely related CUG-Ser clade members (blue: C. tenuis (Cten), D. hansenii (Dhan), H. burtonii (Hbur), C. tanzawaensis (Ctan), Sp. passalidarum (Spal) and S. cerevisiae S288c reference genome (Scer). (c) Scaffolds representing nuclear genome: predicted genes (black lines) and predicted repeats (red lines). (d) Circular mitochondrial genome: predicted genes, tRNAs and rRNAs, sequencing coverage, GC content and sequence similarity to C. lusitaniae, D. hansenii and S. cerevisiae mitochondrial genomes.
Figure 2.
Figure 2.
Tandem gene duplication for adaptation to low nitrogen environment. (a) Enriched gene ontology categories for the 227 unique tandem duplicated genes in M. reukaufii genome. (b) Schematic of GAP1 and PUT4 duplications compared to S. cerevisiae and C. lusitaniae homologues and (c) associated protein sequence phylogenetic tree showing expansion of amino acid permeases in M. reukaufii, with bootstrap supports from RaxML (blue) and PAUP* (black) associated with each numbered node (red). Panel (d) predicted amine oxidase (AOC) homologues (yellow) arranged in TGAs in M. reukaufii compared across syntenic regions on M. bicuspidata and C. lusitaniae. Shaded areas link conserved regions across the genomes of the three species.
Figure 3.
Figure 3.
Amino acid scavenging genes for priority effects caused by nitrogen pre-emption. (a) Expression of four GAP1 homologues of M. reukaufii cells growing for 4 h in either synthetic nectar (20% sucrose) with 0.04 mM proline or glutamine as nitrogen source or YM (approx. 400 mM mixed amino acids) compared to HIP1. All GAP1 homologues are expressed in nectar, but repressed in YM media. (b) NCR of GAP1 genes in M. reukaufii cells growing for 4 h in 20% sucrose supplemented with 0.04, 0.4, 4 or 8 mM of the poor (proline), good (glutamine) and non-amino acid (urea) nitrogen source. Expression of GAP1 homologues, but not HIP1, is strongly repressed by glutamine, and to a much lower extent by proline and urea. Data show mean ± s.d. relative to 0.04 mM concentrations; n = 3 biological replica each with two technical replica. (c) (left panel) Growth of the 2-day late-arriving C. rancensis was significantly repressed in the presence of early arriving M. reukaufii when either no nutrients were restocked (Padj = 5 × 10−7) or only sucrose was restocked (Padj = 15 × 10−6) (10 mg ml−1 per day after C. rancensis arrival). This effect was reversed when 40 mM amino acids were supplied daily post C. rancensis arrival (Padj = 0.646). No observed significant difference between their population densities when grown alone (Padj = 0.221) (right panel). Data show mean ± s.e.
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