Phylogenetic Patterns in the Microbial Response to Resource Availability: Amino Acid Incorporation in San Francisco Bay

<div><p>Aquatic microorganisms are typically identified as either oligotrophic or copiotrophic, representing trophic strategies adapted to low or high nutrient concentrations, respectively. Here, we sought to take steps towards identifying these and additional adaptations to nutrient availability with a quantitative analysis of microbial resource use in mixed communities. We incubated an estuarine microbial community with stable isotope labeled amino acids (AAs) at concentrations spanning three orders of magnitude, followed by taxon-specific quantitation of isotopic incorporation using NanoSIMS analysis of high-density microarrays. The resulting data revealed that trophic response to AA availability falls along a continuum between copiotrophy and oligotrophy, and high and low activity. To illustrate strategies along this continuum more simply, we statistically categorized microbial taxa among three trophic types, based on their incorporation responses to increasing resource concentration. The data indicated that taxa with copiotrophic-like resource use were not necessarily the most active, and taxa with oligotrophic-like resource use were not always the least active. Two of the trophic strategies were not randomly distributed throughout a 16S rDNA phylogeny, suggesting they are under selective pressure in this ecosystem and that a link exists between evolutionary relatedness and substrate affinity. The diversity of strategies to adapt to differences in resource availability highlights the need to expand our understanding of microbial interactions with organic matter in order to better predict microbial responses to a changing environment.</p></div

Pairwise comparisons of isotopic incorporation of ¹⁵N labeled AAs by 107 16S rRNA phylotypes from SF Bay at two concentrations (high, 5 micromolar and low, 50 nanomolar).

<p>Each data point represents the HCE (hybridization corrected enrichment) for a probe set (the slope of delta permil divided by fluorescence). Error bars indicate two standard errors of the slope calculation. The black line represents the linear regression and the blue the 1 to l line.</p

Ternary plot graphically depicting the ratios of the rRNA phylotype-specific incorporation to varying AA concentrations added to SF Bay water.

<p>Data are color-coded according to the trophic strategies identified in Fig. 3. The position of each data point in relation to the three corners represents the relative contribution of each concentration response.</p

Amino acid incorporation trophic strategies mapped onto a maximum parsimony unrooted 16S rRNA gene phylogeny of taxa from a SF Bay seawater sample.

<p>Ancestral states were identified by parsimony. Asterisks indicate strategies with a statistically clustered distribution indicating a phylogenetic signal.</p