Alga-Derived Substrates Select for Distinct Betaproteobacterial Lineages and Contribute to Niche Separation in Limnohabitans Strains

Abstract

We examined the proportions of major Betaproteobacteria subgroups within bacterial communities in diverse nonaxenic, monospecific cultures of algae or cyanobacteria: four species of cryptophyta (genera Cryptomonas and Rhodomonas), four species of chlorophyta (genera Pediastrum, Staurastrum, and Chlamydomonas), and two species of cyanobacteria (genera Dolichospermum and Aphanizomenon). In the cryptophyta cultures, Betaproteobacteria represented 48 to 71% of total bacteria, the genus Limnohabitans represented 18 to 26%, and the Polynucleobacter B subcluster represented 5 to 16%. In the taxonomically diverse chlorophyta group, the genus Limnohabitans accounted for 7 to 45% of total bacteria. In contrast, cyanobacterial cultures contained significantly lower proportions of the Limnohabitans bacteria (1 to 3% of the total) than the cryptophyta and chlorophyta cultures. Notably, largely absent in all of the cultures was Polynucleobacter necessarius (Polynucleobacter C subcluster). Subsequently, we examined the growth of Limnohabitans strains in the presence of different algae or their extracellular products (EPP). Two strains, affiliated with Limnohabitans planktonicus and Limnohabitans parvus, were separately inoculated into axenic cultures of three algal species growing in an inorganic medium: Cryptomonas sp., Chlamydomonas noctigama, and Pediastrum boryanum. The Limnohabitans strains cocultured with these algae or inoculated into their EPP consistently showed (i) pronounced population growth compared to the control without the algae or EPP and (ii) stronger growth stimulation of L. planktonicus than of L. parvus. Overall, growth responses of the Limnohabitans strains cultured with algae were highly species specific, which suggests a pronounced niche separation between two closely related Limnohabitans species likely mediated by different abilities to utilize the substrates produced by different algal species.There is compelling evidence that phytoplankton community dynamics have a significant impact on the composition of bacterioplankton communities (for example, see references 6, 19, and 21). The apparent driving force of such alga-bacterium interactions is likely the nature and quantity of alga-derived substrates available in the form of extracellular phytoplankton products (EPP) or decaying algal biomass. Although it is usually not known which algal species are the major EPP producers in situ, tight species-specific alga-bacterium relationships have been suggested as characterizing bacterium-alga consortia (e.g., 6, 21, 33). Interactions of phytoplankton and bacteria range from symbiotic to parasitic relationships (3). It is not surprising, then, that specific bacterial assemblages associated with different algae can also stimulate or even inhibit algal growth, as documented for cultures of marine diatoms (6). The latter study also demonstrated that free-living and phytoplankton-associated (i.e., attached to algal surfaces) bacteria are significantly different from each other and are dominated by distinct phylog...

Differential freshwater flagellate community response to bacterial food quality with a focus on Limnohabitans bacteria

“…Limnohabitans bacteria are abundant in circum neutral or alkaline lakes (Š imek et al, 2010), they display high growth rates and metabolic flexibility, with a notably tight relationship to algal-derived organic substances and algal exudates (Peréz and Sommaruga, 2006;Š imek et al, 2011). Their high growth potential and a significant contribution to bulk bacterioplankton biomass are counterbalanced by a marked vulnerability to protist grazing (Jezbera et al, 2005;Š imek et al, 2006;Salcher et al, 2008).…”

Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring

“…Many of these studies, however, have been performed in mar ine waters or in laboratory studies (e.g. Grossart et al 2005, Rink et al 2011, Šimek et al 2011, whereas in freshwater ecosystems, only a few studies have investigated these interactions in situ or in field experiments with a high temporal resolution (Salcher et al 2010, Eckert et al 2012. Hence, there is a great need for more intensive studies of the relationship between phytoplankton blooms and shortterm changes of BCC in freshwater ecosystems, especially in spring, when environmental variables rapidly change.…”

Prey-Specific Growth Responses of Freshwater Flagellate Communities Induced by Morphologically Distinct Bacteria from the Genus Limnohabitans

“…Limnohabitans bacteria are abundant opportunistic strategists with high growth and loss rates that quickly respond to sudden pulses of organic carbon of algal origin (16,18,19,21), as well as to enhanced flagellate grazing pressures (9,28). This genus was well represented in our study sites, accounting for ϳ8 to 14% of total bacteria at t 0 (Table 2).…”

“…However, they have been also found as microflora in the digestive tract of algivorous Daphnia magna (22) or as epibionts in filter combs of Daphia galeata (23). Thus, it seems that the main substrates supporting their rapid growth in situ are alga-derived substances (19,24,25). This has also been suggested for several phylogenetically narrow lineages of Flavobacteria (6,7,9).…”

“…The Limnohabitans genus is composed of five major lineages. Four are the so-called R-BT bacteria, which are identified via hybridization with the R-BT065 phylogenetic probe (19), and one lineage, known as LimA, does not hybridize with the probe (18). The four lineages of the R-BT cluster are represented by rapidly growing, morphologically diverse phylotypes with generally opportunistic life strategies (18,20,21).…”