Gut microbiota assemblages of generalist predators are driven by local- and landscape-scale factors
This article has been Reviewed by the following groups
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Abstract
The gut microbiomes of arthropods are reported to have significant impact on key physiological functions such as nutrition, reproduction, behavior, and health. Spiders are diverse and numerically dominant predators in crop fields where they are potentially important regulators of pests. The taxonomic structure of spider gut microbiomes, and environmental drivers of composition are unknown. Harnessing spiders to support agricultural productivity is likely to be supported by an understanding of the gut microbiomes of these predators. This study aimed to deciphering the gut microbiome assembly of predators as well as elucidating the potential implications of key environmental constraints in this process. Here, we used high-throughput sequencing to examine for the first time how the assemblages of bacteria in the gut of spiders are shaped by diverse environmental variables. A total of 27 bacterial phyla were detected with Proteobacteria and Firmicutes dominant. The core bacterial communities included the families Enterobacteriaceae, Chloroplast, Lactobacillaceae, Pseudomonadaceae, Lachnospiraceae, Leuconostocaceae and Ruminococcaceae. Local drivers of microbiome composition were the globally-relevant input use system (organic production versus conventional practice), and crop identity (Chinese cabbage versus cauliflower). Landscape-scale factors, proportion of forest and grassland, compositional diversity, and habitat edge density, also strongly affected gut microbiota. Specific bacterial taxa were enriched in the gut of spiders sampled from different settings and seasons. These findings provide a comprehensive insight into the composition and plasticity of spider gut microbiota. Understanding the temporal responses of specific microbiota could lead to innovative strategies development for boosting biological control services of predators.
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This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/7335614.
This review was performed by a pre-review journal club of ecologists including grad students, undergraduates, and post docs at the University of Washington Seattle campus. We were interested in this paper due to the intersections between microbiology and ecology.
Review Authors: Fiona Boardman, Annie Colgan, Chuck Flaherty, Sanford Leake, Grace Leuchtenberger, Rachel Potter, Monica Sheffer, Julia Smith
In this article, the authors add important data on spider microbiomes to the literature, identify environmental factors affecting the bacterial assemblage at both the local and landscape levels, and gesture towards ecosystem impacts relevant to crops. This was accomplished through the …
This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/7335614.
This review was performed by a pre-review journal club of ecologists including grad students, undergraduates, and post docs at the University of Washington Seattle campus. We were interested in this paper due to the intersections between microbiology and ecology.
Review Authors: Fiona Boardman, Annie Colgan, Chuck Flaherty, Sanford Leake, Grace Leuchtenberger, Rachel Potter, Monica Sheffer, Julia Smith
In this article, the authors add important data on spider microbiomes to the literature, identify environmental factors affecting the bacterial assemblage at both the local and landscape levels, and gesture towards ecosystem impacts relevant to crops. This was accomplished through the collection of spider specimens at various agricultural locations over the four main seasons expressing varying crop compositions of Brassica crops (namely, Chinese Cabbage and Cauliflower), pesticide usages, and land compositions. These specimens were then pooled and sampled via PCR based amplification of bacterial DNA and analysis of identified bacterial DNA segments. This led to the findings that bacterial diversity varied over all such factors, with the variety being more expressed with certain variables/conditions, indicating that the environment of these spiders affects the microbial diversity within their gut microbiome. Our pre-review group appreciates the contribution to a growing literature of spider microbiology and the interesting implications, but we have technical concerns (sequence controls and sample size) and suggestions regarding the structure and content of the introduction and discussion sections.
Major concerns:
1. Controls: The authors don't refer to negative and positive sequencing controls in their methods. It is unclear whether they used controls. A negative control would help detect if there were contamination in the samples. A positive control ensures each step of the process is going as planned and can help detect abundance (see also minor concern 1). Without these it is hard for the reader to be confident in the results.
2. Sample size: The sample size seems small. The authors should justify their sample sizes of the different treatments and their choice to pool spiders. Is there a measure of variability within a site?
3. Data availability: The authors should note in the paper where readers can find their raw sequence data (i.e. uploaded to NCBI or SILVA).
Minor concerns:
1. For abundance assays, the authors used PCR which will not be standard between species. This bias will directly skew the abundance output, and the authors should acknowledge that in the article.
2. The authors may be missing some background on spider microbiomes. Here are several citations that may be good to add (note especially #3 for influence of prey on gut microbiome):
1) Busck, M. M., Settepani, V., Bechsgaard, J., Lund, M. B., Bilde, T., & Schramm, A. (2020). Microbiomes and Specific Symbionts of Social Spiders: Compositional Patterns in Host Species, Populations, and Nests. Frontiers in microbiology, 11, 1845.
2) Goodacre, S.L.; Martin, O.Y.; Bonte, D.; Hutchings, L.; Woolley, C.; Ibrahim, K.; George Thomas, C.; Hewitt, G.M. Microbial modification of host long-distance dispersal capacity. BMC Biol. 2009, 7, 32.
3) Kennedy, S.R., Tsau, S., Gillespie, R., & Krehenwinkel, H. (2020). Are you what you eat? A highly transient and prey‐influenced gut microbiome in the grey house spider Badumna longinqua. Mol Ecol 29: 1001– 1015.
4) Kumar, V., Tyagi, I., Tyagi, K., & Chandra, K. (2020). Diversity and Structure of Bacterial Communities in the Gut of Spider: Thomisidae and Oxyopidae. Frontiers in Ecology and Evolution, 8, 351.
5) Sheffer, M.M., Uhl, G., Prost, S., Lueders, T., Urich, T., & Bengtsson, M.M. (2020). Tissue- and population-level microbiome analysis of the wasp spider Argiope bruennichi identified a novel dominant bacterial symbiont. Microorganisms, 8, 1, 8.
6) Vanthournout, B.; Swaegers, J.; Hendrickx, F. Spiders do not escape reproductive manipulations by Wolbachia. BMC Evol. Biol. 2011, 11, 15.
7) White, J.A.; Styer, A.; Rosenwald, L.C.; Curry, M.M.; Welch, K.D.; Athey, K.J.; Chapman, E.G. Endosymbiotic bacteria are prevalent and diverse in agricultural spiders. Microb. Ecol. 2019.
8) Yun, Y.; Peng, Y.; Liu, F.; Lei, C. Wolbachia screening in spiders and assessment of horizontal transmission between predator and prey. Neotrop. Entomol. 2011, 40, 164–169.
9) Zhang, L.; Zhang, G.; Yun, Y.; Peng, Y. Bacterial community of a spider, Marpiss magister (Salticidae). 3Biotech 2017, 7, 371.
3. The study species are running spiders which can travel a significant distance. The authors should offer a rationale for why they believe the spiders to be from the fields where they were found, making a comparison of the scales of individual movement and environmental variation.
4. The introduction is sparse, and a lot of the background material in the discussion could go in the introduction to help your reader understand the relevance of your research question. But also much of the discussion involves a lot of speculation and is related to things the authors did not test. The implications and speculation is interesting, but perhaps not the addressable by the study the authors conducted. The authors did not really report much on diversity indices between conventional and organic farms, which is another question they can address/emphasize using their data. They can tie these and other factors to community assembly theory.
5. The reasoning behind defining certain variables in a boolean system, namely pesticide usage, is somewhat lacking in explanation. Why was the relative amounts of pesticide usage not estimated or measured?
6. For the seasons, a more precise timing interval could be utilized, or the general timeframe of these seasons relative to specimen collection given more context.
7. Why Euclidean distance? Why Shannon index? Why not compare with other diversity index?
Line edits:
31: "structure of spider microbiomes and…" (delete the comma between microbiomes and the word and)
94: "a range of environmental drives is…" -> "a range of environmental drivers are"
97: "foregoing" -> "aforementioned"
110: Why does the distance of 1 km matter for the establishment of different farming methods? This instead appears to be a factor to prevent ecological overlap and promote diversity as explained later in the sentence, and would be better off by switching the place of the 1 km phrase with the phrase that comes immediately after ("to represent various management systems and crop types")
125: Just has "ref" in place of what is assumed to be a reference?
156: change "were" to "was"
198: Exclude comma after "class"
Sentences running from lines 201 to 205 are redundant with above paragraph
221: "belong" -> "belonging"
254: change form to from
253-254: change "significantly differentially abundant" to "significantly differentiated in abundance"
258 change "significantly differentially dominant" to "significantly differentiated in dominance"
266 change "significantly differentially abundant" to "significantly differentiated in abundance"
267 change "highlighted" to "highlight"
268 change "spider showed" to "spiders show"
272 change "considering of" to "considering"
274 change "gut" to "guts"
275 eliminate dashes (change "landscape-factors" to "landscape factors")
275 end parentheses after "test"
276 end quotations after "'scales'" in phrase "'spatial scales'"
291 eliminate "explaining"
342-345: hard sentence structure to follow, maybe break it up
375 change "found" to "are found"
Fig 4 hard to understand, in caption mention what the points are (OTU? Spider sample?)
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