Microhabitats are associated with diversity-productivity relationships in freshwater bacterial communities

Abstract

Eukaryotic communities commonly display a positive relationship between biodiversity and ecosystem function (BEF) but the results have been mixed when assessed in bacterial communities. Habitat heterogeneity, a factor in eukaryotic BEFs, may explain these variable observations but it has not been thoroughly evaluated in bacterial communities. Here, we examined the impact of habitat on the relationship between diversity assessed based on the (phylogenetic) Hill diversity metrics and heterotrophic productivity. We sampled co-occurring free-living (more homogenous) and particle-associated (more heterogeneous) bacterial habitats in a freshwater, estuarine lake over three seasons: spring, summer and fall. There was a strong, positive, linear relationship between particle-associated bacterial richness and heterotrophic productivity that strengthened when considering dominant taxa. There were no observable BEF trends in free-living bacterial communities for any diversity metric. Biodiversity, richness and Inverse Simpson's index, were the best predictors of particle-associated production whereas pH was the best predictor of free-living production. Our findings show that heterotrophic productivity is positively correlated with the effective number of taxa and that BEF relationships are associated with microhabitats. These results add to the understanding of the highly distinct contributions to diversity and functioning contributed by bacteria in free-living and particle-associated habitats.

Keywords: bacterial communities; biodiversity-ecosystem function; diversity-productivity; heterotrophic productivity; limnology; microhabitats; particle-associated.

Figure 1.

Bacterial counts, community-wide and per-capita heterotrophic production differ between microhabitats. Particle-associated and free-living samples were taken from four stations within Muskegon Lake during 2015 in May, July and September. (A) Free-living bacteria were an order of magnitude (10⁵ cells/mL) more abundant compared to particle-associated bacteria (10⁴ cells/mL). (B) Free-living bacteria were more heterotrophically productive compared to particle-associated bacteria. (C) Particle-associated bacteria were disproportionately heterotrophically productive per cell (expressed in log₁₀(per-capita production)) compared to free-living bacteria.

Figure 2.

Particle-associated diversity tends to be higher than free-living communities, except in ²D (inverse Simpson's index). The y-axis represents the Hill number (^qD) or the unweighted mean pairwise distance (MPD) (grey headers). As the order, q, increases in ^qD from 0 to 2, total, common and dominant taxa are weighted more, respectively. When the unweighted MPD is negative, the total community is phylogenetic clustered whereas if its positive, the community is more phylogenetically overdispersed. ^oD = OTU richness; ¹D = Shannon diversity; ²D = inverse Simpson's index. P-values were corrected for multiple inferences using the Benjamini-Hochberg method from pairwise Wilcoxon rank sum tests.

Figure 3.

⁰D (OTU richness; left) and ²D (inverse Simpson; right) correlate with heterotrophic productivity. Top panel: Biodiversity and community-wide heterotrophic production (μgC/L/day) relationships with (A) ⁰D and (B) ²D. Bottom panel: Biodiversity and log₁₀(per-capita heterotrophic production) (μgC/cell/day) relationships with (C) ⁰D and (D) ²D. Solid lines represent ordinary least squares regression models for significant linear regressions for particle associated (orange) communities. All R² values represent the adjusted R². P-values were corrected for multiple inferences using the Benjamini–Hochberg method.

Figure 4.

Communities with more total lineages (⁰PD or Faith's phylogenetic diversity) tended to be more phylogenetically clustered based on the unweighted mean pairwise distance (MPD). When the unweighted MPD is negative, the total community is phylogenetic clustered whereas if its positive, the community is more phylogenetically overdispersed. R² value represents the adjusted R² from an ordinary least squares regression.