House fly larval grazing alters dairy cattle manure microbial communities

Authors: NEUPANE, SARASWOTI - Kansas State University; SASKI, CHRISTOPHER - Clemson University; Nayduch, Dana

Submitted to: BMC Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/7/2021
Publication Date: 12/15/2021
Citation: Neupane, S., Saski, C.A., Nayduch, D. 2021. House fly larval grazing alters dairy cattle manure microbial communities. BMC Microbiology. 21:1-14. https://doi.org/10.1186/s12866-021-02418-5.
DOI: https://doi.org/10.1186/s12866-021-02418-5

Interpretive Summary: House fly larvae develop in cattle manure, which is rich in organic matter and microorganisms. The larvae feed on both the manure and the various microbes residing therein because they require a live microbial community for successful development. Over time, microbial communities change due to decomposition of the manure substrate, either with or without larvae present. However, when fly larvae are present, they ingest and therefore remove certain microbes, changing the communities in ways not attributable to aging alone. In this study, we characterized the microbial communities of dairy cattle manure and evaluated the changes in those communities over time by comparing the communities in fresh dairy cattle manure to manure that was aged with or without house fly larvae present. We utilized high-throughput sequencing of specific microbial genes to characterize those microbial communities, which allowed us to determine changes to bacteria, archaea (another type of prokaryotic microbe) and protists over time. Bacteria, archaea and protist community compositions significantly differed across fresh, aged, larval-grazed manure. Not surprisingly, aging of manure significantly changed some components of the microbial community. However, we determined that house fly larval grazing made significant impacts on microbes not accounted for by aging alone, particularly certain categories of bacteria and protists, many of which were associated with the cattle from which the manure originated. Larval grazing also significantly reduced the diversity of bacteria and archaea but surprisingly increased protist diversity. Nutrient composition also was impacted by larval grazing. For example, total carbon and nitrogen decreased in larval grazed manure, and these changes were highly correlated with several of bacterial, archaeal and protist communities, suggesting an interrelationship between the community changes and available manure nutrients. House fly larval grazing altered the abundance and diversity of bacterial, archaeal and protist communities differently than aging alone. Fly larvae likely alter communities both by directly feeding on microbes, eliminating certain taxa while promoting others, and by competing with predatory microbes for available nutrients and microbial prey. Our results provide an understanding of the role house fly larvae play in shaping manure microbial communities as well as insight into what house fly larvae may be utilizing as food sources in the manure substrate. Information extrapolated from this study can be used to develop manure management strategies that interfere with house fly development and reduce house fly populations in livestock operations.

Technical Abstract: Background House fly larvae require a live microbial community to successfully develop. Cattle manure is rich in organic matter and microorganisms, comprising a suitable substrate for larvae who feed on both the decomposing manure and the prokaryotic and eukaryotic microbes therein. Microbial communities change as manure ages, and when fly larvae are present changes attributable to larval grazing also occur. Here, we used high throughput sequencing of 16S and 18S rRNA genes to characterize microbial communities in dairy cattle manure and evaluated the changes in those communities over time by comparing the communities in fresh manure to aged manure with or without house fly larvae. Results Bacteria, archaea and protist community compositions significantly differed across manure types (e.g. fresh, aged, larval-grazed). Irrespective of manure type, microbial communities were dominated by the following phyla: Euryarchaeota (Archaea); Proteobacteria, Firmicutes and Bacteroidetes (Bacteria); Ciliophora, Metamonanda, Ochrophyta, Apicomplexa, Discoba, Lobosa and Cercozoa (Protists). Larval grazing significantly reduced the abundances of Bacteroidetes, Ciliophora, Cercozoa and increased the abundances of Apicomplexa and Discoba. Manure aging alone significantly altered the abundance bacteria (Acinetobacter, Clostridium, Petrimonas, Succinovibro), protists (Buxtonella, Enteromonas) and archaea (Methanosphaera and Methanomassiliicoccus). Larval grazing also altered the abundance of several bacterial genera (Pseudomonas, Bacteroides, Flavobacterium, Taibaiella, Sphingopyxis, Sphingobacterium), protists (Oxytricha, Cercomonas, Colpodella, Parabodo) and archaea (Methanobrevibacter and Methanocorpusculum). Overall, larval grazing significantly reduced bacterial and archaeal diversities but increased protist diversity. Moreover, total carbon (TC) and nitrogen (TN) decreased in larval grazed manure, and both TC and TN were highly correlated with several of bacterial, archaeal and protist communities. Conclusions House fly larval grazing altered the abundance and diversity of bacterial, archaeal and protist communities differently than manure aging alone. Fly larvae likely alter community composition by directly feeding on and eliminating microbes and by competing with predatory microbes for available nutrients and microbial prey. Our results lend insight into the role house fly larvae play in shaping manure microbial communities and help identify microbes that house fly larvae utilize as food sources in manure. Information extrapolated from this study can be used to develop manure management strategies to interfere with house fly development and reduce house fly populations.