In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake

Abstract

The substrate partitioning of sympatric populations of freshwater bacterioplankton was studied via microautoradiography and fluorescence in situ hybridization. Fourteen radiolabeled tracers were used to assess microbial acquisition spectra of low-molecular-weight (LMW) organic compounds. The most abundant group, ac1 Actinobacteria, were highly active in leucine, thymidine and glucose assimilation, whereas Alphaproteobacteria from the LD12 lineage (the freshwater sister clade of SAR11) only weakly incorporated these tracers, but exhibited a distinct preference for glutamine and glutamate. Different Bacteroidetes showed contrasting uptake patterns: Flavobacteriales did not incorporate significant amounts of any LMW compound, and Cyclobacteriaceae were clearly specialized on leucine, glucose and arginine. Betaproteobacteria represented the most active and versatile bacterioplankton fraction and 490% of them could be assigned to eight species-to genuslike populations with contrasting substrate specialization. Limnohabitans sp. were the most abundant and active Betaproteobacteria, incorporating almost all tracers. While three closely related betaproteobacterial populations substantially differed in their uptake spectra, two more distantly related lineages had very similar preferences, and one population did not incorporate any tracer. The dominant phototrophic microorganism, the filamentous cyanobacterium Planktothrix rubescens, assimilated several substrates, whereas other (pico)cyanobacteria had no heterotrophic activity. The variable extent of specialization by the studied bacterial taxa on subsets of LMW compounds contrasts theoretical considerations about non-selective microbial substrate assimilation at oligotrophic conditions. This physiological niche separation might be one explanation for the coexistence of freshwater bacterioplankton species in a seemingly uniform environment.

Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage

“…The polyamine transporters are likely being used for putrescine uptake, as the SAGs harbor downstream pathways for its eventual conversion to succinate via the transamination pathway (Dasu et al, 2006;Chou et al, 2008); (Figure 2). Genes for the uptake of carboxylic acids in acI-A1, acI-A7 and acI-B1 were not found in any of the sequenced genomes, consistent with MAR-FISH-based studies (Buck et al, 2009;Salcher et al, 2013).…”

“…As noted for AAA027-L06, the SAGs seem capable of metabolizing glucose but lack an obvious glucose transport system. This is curious in light of MAR-FISH-based studies clearly demonstrating the ability of acI to incorporate glucose (Buck et al, 2009;Salcher et al, 2013). However, most SAGs did contain ABC-type sugar transport components (for example, COG1653) ( Table 2 and Supplementary Table S5) and using the Transporter Classification Database (Saier et al, 2009), a periplasmic component with closest match to the glucose-binding protein in Thermus thermophilus (TC#3.A.1.1.24) was found in eight SAGs but was missing in AAA027-L06.…”

“…They found that Actinobacteria had the highest percentage of cells incorporating leucine but not glucose or acetate, indicating a preference for nitrogen-rich organics. Salcher et al (2013) also found that acI was active in leucine uptake. Some MAR-FISH studies have suggested that another nitrogen-rich compound, NAG may be an important acI substrate (Beier and Bertilsson, 2011;Eckert et al, 2012Eckert et al, , 2013.…”

“…These studies have shown that acI members can take up glucose (Buck et al, 2009), leucine (Buck et al, 2009;Perez et al, 2010;Salcher et al, 2010;Eckert et al, 2012), acetate (Buck et al, 2009), thymidine (Perez et al, 2010), N-acetylglucosamine (NAG) (Beier and Bertilsson, 2011;Eckert et al, 2012) and di-NAG (Beier and Bertilsson, 2011;Eckert et al, 2012;Tada and Grossart, 2014). A recent MAR-FISH study performed on fall samples from Lake Zü rich in Switzerland showed that acI bacteria consumed an amino acid mixture as well (Salcher et al, 2013). The acI in this study did not take up acetate, fructose, arginine, aspartate, glutamate, glutamine, serine, glycine or alanine.…”

Climate‐related changes of soil characteristics affect bacterial community composition and function of high altitude and latitude lakes

“…In any case, it is evident that bacteria interact in a complex way, partly depending on competition for or facilitation of resource utilization (Fuhrman et al ., 2015). It can be assumed that the effects of soil source on bacterial community composition and succession were direct and mediated through a combination of ecological lifestyles (copiotrophs vs. oligotrophs) and taxon‐specific substrate preferences (specialists vs. generalists) (Cottrell & Kirchman, 2000; Eiler et al ., 2003; Salcher et al ., 2013; Pérez et al ., 2015), as well as through species interactions.…”