All over our planet, macroalgae (a.k.a. seaweeds) form a continuous ribbon along our coasts whose area and primary productivity are similar to the Amazon Forest, therefore representing an important source of organic matter. Marine heterotrophic bacteria are the main drivers of macroalgal biomass degradation and reinjection in higher trophic levels. Previous works focused on the strategies implemented to breakdown purified algal compounds. However, in nature, algal compounds are rarely found as unique substrates: algae are complex living organisms and the cell wall of macroalgal cells can be characterized as a 3D matrix, composed of polysaccharides cross-linked with other constituents such as proteins or phlorotannins. To date, information regarding the recycling of intact algae remains scarce. One can expect whole algal tissue degradation would require highly specialized bacteria and would trigger more complex mechanisms. We hypothesized that such bacteria would act as “pioneers”, initiating the attack of the tissues and exposing new substrate niches for opportunistic community members.

In this study we helped to overcome this bottleneck by culturing Zobellia galactanivorans - our favorite flavobacteria that has, as its name suggests, a pronounced taste for algal polysaccharides - in microcosms with fresh tissue pieces of three different brown algae (Laminaria digitata, Fucus serratus and Ascophyllum nodosum) as the sole carbon source. Armed with our boots and gloves, frolicking on the Roscoff seashore, we collected the precious algae, trying not to slip on one! Prior to inoculation we ensured to remove as much natural epiphytic microbes as possible, while keeping the algae alive, by dipping them in detergent and iodine povidone.

The results published here demonstrate that Z. galactanivorans acts as a pioneer bacterium able to initiate the degradation of the three algal species tested. In particular Z. galactanivorans had a great appetite for L. digitata as it rapidly and completely devoured the kelp tissues. FISH visualization is consistent with this observed disintegration as bacterial cells progressively colonized the algal surface and ended up deeply penetrating within the tissues. Interestingly, however, physical contact between bacteria and target algae is not required to observe a disruption of the tissues, revealing that the first steps of the degradation largely relied on the action of extracellular enzymes. Such secreted enzymes could possibly act as public goods shared with opportunist bacteria less equipped enzymatically. Indeed, we demonstrated using co-cultures that Z. galactanivorans might display a sharing behavior by favoring the growth of a non-degrading Tenacibaculum sp. strain. 

We further studied the full transcriptome of Z. galactanivorans during the exponential phase of the algal degradation (RNA-seq). Compared to the degradation of unique algal polysaccharides, the growth with fresh tissues triggered the expression of specific loci dedicated to polysaccharide utilization and secretion systems, highlighting their key role in the degradation processes and the need to further characterize them. Interestingly, the attack of fresh algae also induced pronounced bacterial responses to cope with stress. Indeed, algae do not surrender easily and bacterial degraders need to be well equipped to resist the algal defense mechanisms. Those results, combined with comparative genomic and growth experiments within the genus Zobellia, shed light on overlooked metabolic mechanisms that might be essential features of pioneer bacteria.

This study provides the first insights into the metabolic strategies of pioneer bacteria during fresh macroalgae utilization. Altogether, our results raised the relevance to consider the full complexity of whole macroalgae tissues in further degradation studies, as it would take a step forward in the understanding of the algal biomass recycling through the identification of new metabolic pathways or the characterization of bacterial cooperative interactions.

For full details, check our new paper at: https://www.nature.com/articles/s41396-022-01251-6

Twitter: @FThomas_Roscoff  and @mae_brunet