Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes

Abstract

Adaptive radiations are important drivers of niche filling, since they rapidly adapt a single clade of organisms to ecological opportunities. Although thought to be common for animals and plants, adaptive radiations have remained difficult to document for microbes in the wild. Here we describe a recent adaptive radiation leading to fine-scale ecophysiological differentiation in the degradation of an algal glycan in a clade of closely related marine bacteria. Horizontal gene transfer is the primary driver in the diversification of the pathway leading to several ecophysiologically differentiated Vibrionaceae populations adapted to different physical forms of alginate. Pathway architecture is predictive of function and ecology, underscoring that horizontal gene transfer without extensive regulatory changes can rapidly assemble fully functional pathways in microbes.

Genetic analyses unravel the crucial role of a horizontally acquired alginate lyase for brown algal biomass degradation by Zobellia galactanivorans

“…Similarly, several genes involved in the degradation of red algal porphyran and agar were transferred from a marine bacterium to gut bacteria of surgeonfish (Rebuffet et al, 2011) and humans (Hehemann, 2010). Recently, analysis of a clade of Vibrionaceae revealed a complex series of independent acquisitions and transfers of alginate lyases and oligoalginate lyases between closely related populations, leading to fine-scale differentiation of the alginolytic potential (Hehemann et al, 2016). Here, we show that addition of a single exogenous gene to a pre-existing alginolytic system could confer an adaptive advantage on Z. galactanivorans by improving access to alginate gels and increasing its ability to degrade fresh algal biomass.…”

“…In the environment, polysaccharide degradation is thought to involve at least three ecophysiological types of bacteria: (i) pioneers, which have full degradation pathways and secrete soluble enzymes that break down polymers and produce diffusible products (ii) harvesters, which possess a complete set of degradation enzymes but do not secrete soluble enzymes and may benefit from the soluble enzymes secreted by pioneers and (iii) scavengers, which lack enzymes that cleave polysaccharides but can use small oligomers released by pioneers and harvesters (Hehemann et al, 2016). The presence of AlyA1containing bacteria acting as pioneers for the initial attack on algal biomass could influence community assembly by exposing new substrate niches for harvesters and scavengers.…”

Natural resource landscapes of a marine bacterium reveal distinct fitness‐determining genes across the genome

“…9CS106 has a battery of seven alginate lyases; disruption of any one does not have a measurable fitness effect. We have shown recently that gene dosage directly translates into increased activity, which may be important in competitive situations (Hehemann et al ., ) but under the pure culture conditions chosen here high gene dosage is sufficiently redundant. Nonetheless, even in the environment, selection on redundant pathways will be weaker and may thus be an important factor in allowing the horizontal acquisition of slightly deleterious alleles or genes that can subsequently be optimized by mutation and selection.…”

“…F13, which has been found to be a generalist with regard to habitat association (Preheim et al, 2011), does not utilize the same resources in different habitats; instead, it exploits distinct resources depending on habitat; (2) habitat complexity strongly buffers mutant fitness costs, indicating less of a reliance on any one gene when many substrates are available; and (3) the loss of anabolic genes in these resource spectra is more detrimental than the loss of catabolic genes, perhaps due to redundancy of catabolic pathways. Redundancy of catabolic genes is adaptive to rapid growth under replete conditions, since it enables rapid ramping up of activity and can provide a competitive advantage during exploitation of resource pulses (Hehemann et al, 2016;Roller et al, 2016). Such conditions may capture an ecologically important life stage for vibrios.…”

“…F13, which associates with dead zooplankton and brown algal detritus (Preheim et al, 2011;Hehemann et al, 2016). While several metabolic traits across all vibrios, such as the degradation of chitin, suggest that the association with zooplankton is ancestral in vibrios (Hunt et al, 2008a), their ability to degrade algal polysaccharides is due to a series of very recent horizontal gene transfer events (Hehemann et al, 2016). Because these constituent resources of these habitats can be recreated in the lab, we use this model to ask: Does this generalist exploit the same resources and thus require the same genes and pathways across habitats?…”