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Evaluation of Rnalater™ As a Field-Compatible Preservation Method For bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448770; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Evaluation of RNAlater™ as a field-compatible preservation method for 2 metaproteomic analyses of bacteria-animal symbioses 3 Authors: Marlene Jensen1, Juliane Wippler2, Manuel Kleiner1 4 Affiliations: 5 1: North Carolina State University; Department of Plant & Microbial Biology, 112 Derieux Pl, 4510 6 Thomas Hall, Raleigh, NC 27695 7 2: Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, 8 Bremen, Germany 9 Correspondence: 10 manuel_kleiner(at)ncsu(dot)edu 11 mjensen2(at)ncsu(dot)edu 12 Keywords: mass spectrometry, 1D-LC-MS/MS, microbial communities, preservation methods, 13 microbiome, field sampling, environmental microbiology 14 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448770; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 15 Abstract 16 Field studies are central to environmental microbiology and microbial ecology as they enable studies 17 of natural microbial communities. Metaproteomics, the study of protein abundances in microbial 18 communities, allows to study these communities ‘in situ’ which requires protein preservation directly 19 in the field as protein abundance patterns can change rapidly after sampling. Ideally, a protein 20 preservative for field deployment works rapidly and preserves the whole proteome, is stable in long- 21 term storage, is non-hazardous and easy to transport, and is available at low cost. Although these 22 requirements might be met by several protein preservatives, an assessment of their suitability in field 23 conditions when targeted for metaproteomics is currently lacking. Here, we compared the protein 24 preservation performance of flash freezing and the preservation solution RNAlater™ using the 25 marine gutless oligochaete Olavius algarvensis and its symbiotic microbes as a test case. In addition, we 26 evaluated long-term RNAlater™ storage after 1 day, 1 week and 4 weeks at room temperature (22-23 27 °C). We evaluated protein preservation using one dimensional liquid chromatography tandem mass 28 spectrometry (1D-LC-MS/MS). We found that RNAlater™ and flash freezing preserved proteins 29 equally well in terms of total number of identified proteins or relative abundances of individual 30 proteins and none of the test time points were altered compared to t0. Moreover, we did not find 31 biases against specific taxonomic groups or proteins with particular biochemical properties. Based 32 on our metaproteomics data and the logistical requirements for field deployment we recommend 33 RNAlater™ for protein preservation of field-collected samples when targeted for metaproteomcis. 34 Importance 35 Metaproteomics, the large-scale identification and quantification of proteins from microbial 36 communities, provides direct insights into the phenotypes of microorganisms on the molecular level. 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448770; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 37 To ensure the integrity of the metaproteomic data, samples need to be preserved immediately after 38 sampling to avoid changes in protein abundance patterns. In laboratory set-ups samples for 39 proteomic analyses are most commonly preserved by flash freezing; however, liquid nitrogen or dry 40 ice is often unavailable at remote field locations due to its hazardous nature and transport 41 restrictions. Our study shows that RNAlater™ can serve as a low hazard, easy to transport 42 alternative to flash freezing for field preservation of samples for metaproteomics. We show that 43 RNAlater™ preserves the metaproteome equally well as compared to flash freezing and protein 44 abundance patterns remain stable during long-term storage for at least 4 weeks at room temperature. 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448770; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 45 Introduction 46 Field studies are central to environmental microbiology and microbial ecology as they allow for the 47 in situ study of microbial communities and their interactions with the biotic and abiotic environment. 48 This includes the study of symbiotic interactions between microorganisms and animal or plant hosts. 49 Many of the approaches used to study these symbioses “in situ” in reality require that samples are 50 preserved in the field for later analysis in the laboratory. This includes, for example, cell counting of 51 specific taxa using fluorescence in situ hybridization (FISH) methods [1–3] and various sequencing 52 based approaches for the characterization of taxonomic community structure and functional 53 potential such as 16S rRNA gene sequencing [4–6] and shotgun metagenomics [7–11]. Sample 54 preservation methods for most of these approaches have been established over the last few decades 55 [12–14]. However, for some approaches, including metaproteomics, field preservation methods have 56 not been extensively investigated. 57 Metaproteomics is an umbrella term that encompasses approaches for the large-scale identification 58 and quantification of expressed proteins in a microbial community [15, 16]. Metaproteomics can be 59 used not only to determine the metabolism and physiology of community members but also to 60 estimate community member abundances, interactions and carbon sources [16–18]. Over the last 61 decade metaproteomics has led to many significant discoveries including novel insights into 62 microbial biofilm communities collected from acid mine drainages (AMD) [19, 20], marine 63 symbioses [11, 21, 22], soil communities [23, 24] and the human gut microbiota [25–27]. 64 One critical consideration for field-based metaproteomics studies is the preservation of in situ gene 65 expression patterns by stopping biological activity in the samples. In contrast to DNA-based 66 approaches such as 16S rRNA gene sequencing and shotgun metagenomics, for which outcomes 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448770; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 67 only change if cell numbers in the sample change considerably through cell growth and division, 68 protein abundances in cells can change more quickly in response to changing environmental 69 conditions and thus fast preservation in the field is essential for an accurate snapshot of community 70 activity. The time windows in which protein abundance changes are detectable varies greatly 71 between species. For example, for the fast growing Escherichia coli, protein abundances have been 72 shown to significantly change within 10-30 minutes after being exposed to environmental stress [28], 73 while changes in slow growing ammonia-oxidizing bacteria take many hours to days to occur [29]. 74 Therefore, sample preservation for metaproteomics should ideally happen within 10 to 30 minutes 75 after removal of a specimen from its environment. While this can easily be achieved in the 76 laboratory, simply by flash freezing the sample, it can be challenging when collecting samples in the 77 field. At remote field sites low-temperature freezers are often unavailable and liquid nitrogen or dry 78 ice for flash freezing are not an option due to transport restrictions to the field site or due to boiling 79 off/sublimation during extended field stays. Therefore, a field compatible method for 80 metaproteomics sample preservation is needed. Such a method should: i) immediately stop 81 biological activity and thus prevent changes in gene expression and protein degradation, ii) preserve 82 the whole metaproteome without bias against specific protein types or taxonomic groups, iii) work 83 for extended storage at room temperature, iv) work for a wide range of sample types and species, v) 84 be non-hazardous and easy to transport, and vi) be available at low cost. 85 Various studies have evaluated field-compatible preservation methods for nucleic acids in a wide 86 variety of sample types [14, 30, 31]. In contrast, only limited work has been done on field 87 preservation of proteins and, to our knowledge, only for a single cultured bacterial species [32]. Saito 88 et al. examined the performance of SDS extraction buffer, ethanol, trichloroacetic acid (TCA), B- 89 PER and RNAlater™ to preserve cultures of the marine cyanobacterium Synechococcus using flash 90 frozen samples as a control. The test samples were stored at room temperature (RT) for 4 weeks. 5 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448770; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 91 The authors found that all samples yielded lower protein concentrations compared to their flash 92 frozen control. Despite this, Saito et al. found that for RNAlater™ the number of identified proteins 93 and relative protein abundances were highly similar to flash frozen controls while the remaining 94 preservatives showed significantly lower protein identification numbers.
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