Effects of interspecies interactions on marine community ecosystem function

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Abstract

Microbial communities perform key ecosystem processes collectively. One such process is the degradation of carbohydrate polymers, which are the dominant pool of organic carbon in natural environments. Carbohydrate polymers are often degraded in a stepwise manner. Individual steps are performed by different microbial species, which form trophic cascades with carbon polymers at the bottom and fully oxidised carbon at the top. It is widely believed that these trophic cascades are hierarchically organised, where organisms at each level rely on organisms at the levels below. However, whether and how the higher-level organisms can also affect processes at the lower levels is not well understood. Here we studied how carbohydrate polymer degradation mediated by secreted enzymes is affected by species at higher trophic levels, i.e., species that cannot produce the enzymes for polymer degradation but can grow in presence of the polymer degraders. We used growth and enzyme assays in combination with transcriptomics to study how chitin degradation by a number of Vibrio strains is affected by the presence of different cross-feeders that consume metabolic by-products. We found that interactions between the degraders and cross-feeders influence the rate of chitin degradation by the community. Furthermore, we show that this is a result of changes in chitinase expression by degraders. Overall, our results demonstrate that interactions between species can influence key ecosystem functions performed by individuals within microbial communities. These results challenge the perspective that trophic cascades based on metabolically coupled microbial communities are unidirectional and provide mechanistic insights into these downstream interactions.

Article activity feed

  1. at the bottom

    Since the authors are mentioning the species that degrade the chitin, reaction from which the rest of the trophic chain will cascade, shouldn't that be 'at the top' of the trophic hierarchy instead?

  2. (Figure 4).

    It is known that growth rate directly impacts gene expression, and that sometimes, gene expression changes between two conditions are simply connected to a decreased growth rate in the studied condition. I am wondering if there would be a way to sort out the genes that are associated with differential expression between genes whose expression change is likely related to growth rate effect versus genes whose expression changes are not (based on information that can be found in the litterature).

  3. Figure 3:

    I like the use of a heatmap to represent the data in A. I wonder if the choice of color scale is confusing here, as these three colors are used to represent the three enzyme classes in the rest of the figures. It may be more intuitive to have no change shown in white/gray and positive/negative changes shown in contrasting colors.

    It could also be good to move Figure S2 into a second panel of A here, as it may be nice to directly visually compare the growth impact of interactors to their impact on enzyme activity.

  4. Figure 4:

    Do you also have information about the gene expression changes of the cross-feeder species in these interactive contexts vs. alone? It's not necessary here but it could be interesting/aid in interpretation of what is happening mechanistically.

  5. Figure 5:

    It may make sense to combine figures 5 and 6 here, as they seem to be showing the same information but for the two degrader species. This would make comparing the degrader response easier .

  6. The underlying question we aim to answer is whether bacterial species without the genetic repertoire to perform a given function can influence that function when measured at the level of consortia

    This is a super interesting question!

  7. The underlying question we aim to answer is whether bacterial species without the genetic repertoire to perform a given function can influence that function when measured at the level of consortia

    This is a super interesting question!

  8. (Figure 4).

    It is known that growth rate directly impacts gene expression, and that sometimes, gene expression changes between two conditions are simply connected to a decreased growth rate in the studied condition. I am wondering if there would be a way to sort out the genes that are associated with differential expression between genes whose expression change is likely related to growth rate effect versus genes whose expression changes are not (based on information that can be found in the litterature).

  9. Figure 5:

    It may make sense to combine figures 5 and 6 here, as they seem to be showing the same information but for the two degrader species. This would make comparing the degrader response easier .

  10. Figure 4:

    Do you also have information about the gene expression changes of the cross-feeder species in these interactive contexts vs. alone? It's not necessary here but it could be interesting/aid in interpretation of what is happening mechanistically.

  11. at the bottom

    Since the authors are mentioning the species that degrade the chitin, reaction from which the rest of the trophic chain will cascade, shouldn't that be 'at the top' of the trophic hierarchy instead?

  12. Figure 3:

    I like the use of a heatmap to represent the data in A. I wonder if the choice of color scale is confusing here, as these three colors are used to represent the three enzyme classes in the rest of the figures. It may be more intuitive to have no change shown in white/gray and positive/negative changes shown in contrasting colors.

    It could also be good to move Figure S2 into a second panel of A here, as it may be nice to directly visually compare the growth impact of interactors to their impact on enzyme activity.